Plant Cell Reports

, Volume 32, Issue 2, pp 319–328 | Cite as

The promoter of an A9 homolog from the conifer Cryptomeria japonica imparts male strobilus-dominant expression in transgenic trees

  • Manabu Kurita
  • Ken-ichi Konagaya
  • Atsushi Watanabe
  • Teiji Kondo
  • Katsuaki Ishii
  • Toru Taniguchi
Original Paper

Abstract

Key message

GUS analysis inCryptomeria japonicarevealed that theCjMALE1promoter is activated in the male strobilus ofC. japonica.

Abstract

Toward the development of male sterile technology for Cryptomeria japonica, a male strobilus-dominant promoter of C. japonica was isolated. The CjMALE1 gene was isolated from a male strobilus-specific suppression subtractive hybridization (SSH) library, and the promoter was isolated by the TAIL-PCR method. To characterize the CjMALE1 promoter, β-glucuronidase (GUS)-fused genes were constructed and introduced into C. japonica using Agrobacterium tumefaciens. GUS expression from CjMALE1-2.5 K (2,718 bp fragment)::GUSC. japonica and CjMALE1-1 K (1,029 bp fragment)::GUSC. japonica was detected in the tapetum and microspore mother cells. These promoter fragments were comparably active in the pre-meiotic stage of the male strobilus of C. japonica. Our analysis showed that the 1,029 bp promoter had all the cis-elements necessary for male strobilus-dominant expression of CjMALE1. When CjMALE1-1 K::GUS was introduced into Arabidopsis, GUS expression was detected in the same spatiotemporal pattern as in C. japonica. These results suggest that the CjMALE1 promoter is subject to transcriptional regulatory systems consisting of cis- and trans-elements that have been highly conserved during evolution.

Keywords

Cryptomeria japonica Male strobilus-dominant promoter β-glucuronidase TAIL-PCR Arabidopsis 

Supplementary material

299_2012_1365_MOESM1_ESM.rtf (5 kb)
Supplementary material 1 (RTF 6 kb)

References

  1. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472PubMedCrossRefGoogle Scholar
  2. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869PubMedCrossRefGoogle Scholar
  3. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4:879–887PubMedGoogle Scholar
  4. Brunner A, Li J, DiFazio S, Shevchenko O, Montgomery B, Mohamed R, Wei H, Ma C, Elias A, VanWormer K, Strauss S (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100CrossRefGoogle Scholar
  5. Crossley S, Greenland A, Dickinson H (1995) The characterisation of tapetum-specific cDNAs isolated from a Lilium henryi L. meiocyte subtractive cDNA library. Planta 196:523–529PubMedCrossRefGoogle Scholar
  6. Dickinson HG, Bell P (1972) The role of the tapetum in the formation of sporopollenin-containing structures during microsporogenesis in Pinus banksiana. Planta 107:205–215CrossRefGoogle Scholar
  7. Gallusci P, Salamini F, Thompson R (1994) Differences in cell type-specific expression of the gene Opaque 2 in maize and transgenic tobacco. Mol Gen Genet 244:391–400PubMedCrossRefGoogle Scholar
  8. Goto N, Pharis R (1999) Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Can J Botan 77:944–954CrossRefGoogle Scholar
  9. Grotewold E, Drummond B, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553PubMedCrossRefGoogle Scholar
  10. Gubler F, Raventos N, Keys M, Watts R, Mundy J, Jacobsen J (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17:1–9PubMedCrossRefGoogle Scholar
  11. Hamilton D, Schwarz Y, Mascarenhas J (1998) A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol Biol 38:663–669PubMedCrossRefGoogle Scholar
  12. Hashizume H (1973) Studies on flower bud formation, flower sex differentiation and their control in conifers. Bull. Totori Univ. Forests 7:1–139 (in Japanese & English summary)Google Scholar
  13. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  14. Hofig K, Moyle R, Putterill J, Walter C (2003) Expression analysis of four Pinus radiata male cone promoters in the heterologous host Arabidopsis. Planta 217:858–867PubMedCrossRefGoogle Scholar
  15. Hofig K, Moller R, Donaldson L, Putterill J, Walter C (2006) Towards male sterility in Pinus radiata—a stilbene synthase approach to genetically engineer nuclear male sterility. Plant Biotechnol J 4:333–343PubMedCrossRefGoogle Scholar
  16. Hosoo Y, Yoshii E, Negishi K, Taira H (2005) A histological comparison of the development of pollen and female gametophytes in fertile and sterile Cryptomeria japonica. Sex Plant Reprod 18:81–89CrossRefGoogle Scholar
  17. Hu J, Mitchum M, Barnaby N, Ayele B, Ogawa M, Nam E, Lai W, Hanada A, Alonso J, Ecker J, Swain S, Yamaguchi S, Kamiya Y, Sun T (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20:320–336PubMedCrossRefGoogle Scholar
  18. Itoh H, Ueguchi-Tanaka M, Sentoku N, Kitano H, Matsuoka M, Kobayashi M (2001) Cloning and functional analysis of two gibberellin 3 beta-hydroxylase genes that are differently expressed during the growth of rice. Proc Natl Acad Sci USA 98:8909–8914PubMedCrossRefGoogle Scholar
  19. Jacobsen S, Olszewski N (1991) Characterization of the Arrest in Anther Development Associated with Gibberellin Deficiency of the gib-1 Mutant of Tomato. Plant Physiol 97:409–414PubMedCrossRefGoogle Scholar
  20. Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J 35:104–115PubMedCrossRefGoogle Scholar
  21. Konagaya K, Ando S, Kamachi S, Tsuda M, Tabei Y (2008) Efficient production of genetically engineered, male-sterile Arabidopsis thaliana using anther-specific promoters and genes derived from Brassica oleracea and B. rapa. Plant Cell Rep 27:1741–1754PubMedCrossRefGoogle Scholar
  22. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396CrossRefGoogle Scholar
  23. Kurita M, Taniguchi T, Nakada R, Kondo T, Watanabe A (2011) Spatiotemporal gene expression profiles associated with male strobilus development in Cryptomeria japonica by suppression subtractive hybridization. Breed Sci 61:174–182CrossRefGoogle Scholar
  24. Lemmetyinen J, Keinonen K, Sopanen T (2004) Prevention of the flowering of a tree, silver birch. Mol Breed 13:243–249CrossRefGoogle Scholar
  25. Liu Y, Whittier R (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674–681PubMedCrossRefGoogle Scholar
  26. Luo H, Kausch A, Hu Q, Nelson K, Wipff J, Fricker C, Owen T, Moreno M, Lee J, Hodges T (2005) Controlling transgene escape in GM creeping Bentgrass. Mol Breed 16:185–188CrossRefGoogle Scholar
  27. Maekawa M, Kawamoto T (2002) Intact sectioning of plant tissues with a cryomicrotome. Breed Sci 52:57–60CrossRefGoogle Scholar
  28. Moitra A, Bhatnagar S (1982) Ultrastructure, cytochemical, and histochemical studies on pollen and male gamete development in gymnosperms. Gamete Res 5:71–112CrossRefGoogle Scholar
  29. Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989PubMedCrossRefGoogle Scholar
  30. Nagao A (1985) Floral initiation of Cryptomeria japonica under three different temperature conditions with treatments of various concen- trations of GA3. J Jpn For Soc 67:414–417 (in Japanese with English summary)Google Scholar
  31. Okamura M, Kondo T (1995) Manual for tissue culture of pine. Bull Natl For Tree Breed Center 13:139–143Google Scholar
  32. Paul W, Hodge R, Smartt S, Draper J, Scott R (1992) The isolation and characterisation of the tapetum-specific Arabidopsis thaliana A9 gene. Plant Mol Biol 19:611–622PubMedCrossRefGoogle Scholar
  33. Rogers H, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale D, Twell D (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45:577–585PubMedCrossRefGoogle Scholar
  34. Rubio-Somoza I, Martinez M, Abraham Z, Diaz I, Carbonero P (2006) Ternary complex formation between HvMYBS3 and other factors involved in transcriptional control in barley seeds. Plant J 47:269–281PubMedCrossRefGoogle Scholar
  35. Sanders P, Bui A, Weterings K, McIntire K, Hsu Y, Lee P, Truong M, Beals T, Goldberg R (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322CrossRefGoogle Scholar
  36. Scott R, Dagless E, Hodge R, Paul W, Soufleri I, Draper J (1991) Patterns of gene expression in developing anthers of Brassica napus. Plant Mol Biol 17:195–207PubMedCrossRefGoogle Scholar
  37. Skriver K, Olsen F, Rogers J, Mundy J (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88:7266–7270PubMedCrossRefGoogle Scholar
  38. Solano R, Nieto C, Avila J, Canas L, Diazi Pazares J (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 14:1773–1784PubMedGoogle Scholar
  39. Stalberg K, Ellerstrom M, Sjodahl S, Ezcurra I, Wycliffe P, Rask L (1998) Heterologous and homologous transgenic expression directed by a 2S seed storage promoter of Brassica napus. Transgenic Res 7:165–172CrossRefGoogle Scholar
  40. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant J 34:635–645PubMedCrossRefGoogle Scholar
  41. Swapna L, Khurana R, Vijaya Kumar S, Tyagi AK, Rao KV (2010) Pollen-Specific Expression of Oryza sativa Indica Pollen Allergen Gene (OSIPA) Promoter in Rice and Arabidopsis Transgenic Systems. Mol Biotechnol 48(1):49–59CrossRefGoogle Scholar
  42. Tang W, Perry S (2003) Binding site selection for the plant MADS domain protein AGL15—an in vitro and in vivo study. J Biol Chem 278:28154–28159PubMedCrossRefGoogle Scholar
  43. Taniguchi T, Kurita M, Ohmiya Y, Kondo T (2005) Agrobacterium tumefaciens-mediated transformation of embryogenic tissue and transgenic plant regeneration in Chamaecyparis obtusa Sieb. et Zucc. Plant Cell Rep 23:796–802PubMedCrossRefGoogle Scholar
  44. Taniguchi T, Ohmiya Y, Kurita M, Tsubomura M, Kondo T (2008) Regeneration of transgenic Cryptomeria japonica D. Don after Agrobacterium tumefaciens-mediated transformation of embryogenic tissue. Plant Cell Rep 27:1461–1466PubMedCrossRefGoogle Scholar
  45. Walden A, Walter C, Gardner R (1999) Genes expressed in Pinus radiata male cones include homologs to anther-specific and pathogenesis response genes. Plant Physiol 121:1103–1116PubMedCrossRefGoogle Scholar
  46. Wei H, Meilan R, Brunner A, Skinner J, Ma C, Gandhi H, Strauss S (2007) Field trial detects incomplete barstar attenuation of vegetative cytotoxicity in Populus trees containing a poplar LEAFY promoter: barnase sterility transgene. Mol Breed 19:69–85CrossRefGoogle Scholar
  47. Xu S, Liu G, Chen R (2006) Characterization of an anther- and tapetum-specific gene and its highly specific promoter isolated from tomato. Plant Cell Rep 25:231–240PubMedCrossRefGoogle Scholar
  48. Xu X, Bian J, Liu S, Song H, Shi N, Tao Y, Wang H (2010) Flower-specific expression of Arabidopsis PCS1 driven by AGAMOUS second intron in tobacco decreases the fertility of transgenic plants. Mol Breed 27(3):337–346CrossRefGoogle Scholar
  49. Yuh C, Bolouri H, Davidson E (1998) Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene. Science 279:1896–1902PubMedCrossRefGoogle Scholar
  50. Zhang C, Norris-Caneda KH, Rottmann WH, Gulledge JE, Chang S, Kwan BY, Thomas AM, Mandel LC, Kothera RT, Victor AD, Pearson L, Hinchee MA (2012) Control of Pollen Mediated Gene Flow in Transgenic Trees. Plant Physiology [21 Jun, Epub ahead of print]. doi:10.1104/pp.112.197228

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Manabu Kurita
    • 1
    • 2
  • Ken-ichi Konagaya
    • 2
  • Atsushi Watanabe
    • 3
  • Teiji Kondo
    • 1
  • Katsuaki Ishii
    • 2
  • Toru Taniguchi
    • 1
    • 2
  1. 1.Forestry and Forest Products Research InstituteForest Tree Breeding CenterHitachiJapan
  2. 2.Forestry and Forest Products Research InstituteForest Bio-Research CenterHitachiJapan
  3. 3.Faculty of AgricultureKyushu UniversityFukuokaJapan

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