Skip to main content

Gene Expression Analysis of Aquatic Angiosperms Podostemaceae to Gain Insight into the Evolution of Their Enigmatic Morphology

  • Protocol
  • First Online:
Plant Organogenesis

Part of the book series: Methods in Molecular Biology ((MIMB,volume 959))

Abstract

Podostemaceae is a family of aquatic angiosperms growing submerged on rocks in fast-flowing water and called moss-like or alga-like riverweeds. It evolved remarkable innovations to adapt to such an extreme environment, one of which is reduced shoots borne on roots adhering to rock surface. Recent observations revealed that the basal subfamily Tristichoideae, like most other angiosperms, has typical shoot apical meristems (SAMs). In species of the subfamily Podostemoideae, however, shoot apical meristems (SAMs) are not formed during development and new leaves arise from the meristematic basal region of preexisting leaves. The genetic basis of this shoot organogenesis process, e.g., the expression patterns of genes homologous to transcription factors regulating shoot development, is essential to better understand the evolution of Podostemaceae. A gene expression analysis found that the SAM-less Podostemoideae leaf has mixed identity of SAM and leaf, and provided insight into the evolution of the shoot in Podostemaceae.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Steeves TA, Sussex IM (1989) Patterns in plant development, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  2. Katayama N, Koi S, Kato M (2010) Expression of SHOOT MERISTEMLESS, WUSCHEL, and ASYMMETRIC LEAVES 1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. Plant Cell 22:2131–2140

    Article  PubMed  CAS  Google Scholar 

  3. Rutishauser R (1997) Structural and developmental diversity in Podostemaceae (river-weeds). Aquat Bot 57:29–70

    Article  Google Scholar 

  4. Bell AD (2008) Plant form: an illustrated guide to flowering plant morphology. Timber Press, Portland

    Google Scholar 

  5. van Steenis CGGJ (1981) Rheophytes of the world. Sijthoff & Noordhoff, Alphen aan den Rijn

    Book  Google Scholar 

  6. Jäger-Zürn I (1998) Anatomy of the Hydrostachyaceae. In: Landolt E, Jäger-Zürn I, Schnell RAA (eds) Extreme adaptations in angiospermous hydrophytes. Gebrüder Borntraeger, Berlin

    Google Scholar 

  7. Wurdack KJ, Davis CC (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 96:1551–1570

    Article  PubMed  Google Scholar 

  8. Ruhfel BR et al (2011) Phylogeny of the clusioid clade (Malpighiales): evidence from the plastid and mitochondrial genomes. Am J Bot 98:306–325

    Article  PubMed  Google Scholar 

  9. Soltis DE et al (2011) Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot 98:704–730

    Article  PubMed  Google Scholar 

  10. Cook CDK, Rutishauser R (2007) Podostemaceae. In: Kubitzki K (ed) The families and genera of vascular plants, IX. Springer, Berlin

    Google Scholar 

  11. Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New York

    Google Scholar 

  12. Willis JC (1902) Studies in the morphology and ecology of the Podostemaceae of Ceylon and India. Ann Roy Bot Gar Peradeniya 1:267–465

    Google Scholar 

  13. Mohan Ram HY, Sehgal A (1997) In vitro studies on developmental morphology of Indian Podostemaceae. Aquat Bot 57:97–132

    Article  Google Scholar 

  14. Sehgal A, Sethi M, Mohan Ram HY (2002) Origin, structure, and interpretation of the thallus in Hydrobryopsis sessilis (Podostemaceae). Int J Plant Sci 163:891–905

    Article  Google Scholar 

  15. Suzuki K, Kita Y, Kato M (2002) Comparative developmental anatomy of seedling in nine species of Podostemaceae (subfamily Podostemoideae). Ann Bot 89:755–765

    Article  PubMed  Google Scholar 

  16. Imaichi R, Maeda R, Suzuki K, Kato M (2004) Developmental morphology of foliose shoots and seedlings of Dalzellia zeylanica (Podostemaceae) with special reference to their meristems. Bot J Linn Soc 144:289–302

    Article  Google Scholar 

  17. Koi S, Kato M (2010) Developmental morphology of seedling and shoot and phylogenetic relationship of Diplobryum koyamae (Podostemaceae). Am J Bot 97:373–387

    Article  PubMed  CAS  Google Scholar 

  18. Kita Y, Kato M (2005) Seedling developmental anatomy of an undescribed Malaccotristicha species (Podostemaceae, subfamily Tristichoideae) with implications for body plan evolution. Plant Syst Evol 254:221–232

    Article  Google Scholar 

  19. Ota M, Imaichi R, Kato M (2001) Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). Am J Bot 88:382–390

    Article  PubMed  CAS  Google Scholar 

  20. Koi S, Kato M (2003) Comparative developmental anatomy of the root in three species of Cladopus (Podostemaceae). Ann Bot 91:927–937

    Article  PubMed  Google Scholar 

  21. Hammond BL (1936) Regeneration of Podostemon ceratophyllum. Bot Gaz 97:834–845

    Article  Google Scholar 

  22. Rutishauser R (1995) Developmental patterns of leaves in Podostemaceae compared with more typical flowering plants: saltational evolution and fuzzy morphology. Can J Bot 73:1305–1317

    Article  Google Scholar 

  23. Rutishauser R, Grubert M (1999) The architecture of Mourera fluviatilis (Podostemaceae): developmental morphology of inflorescences, flowers, and seedlings. Am J Bot 86:907–922

    Article  PubMed  CAS  Google Scholar 

  24. Rutishauser R, Grubert M (2000) Developmental morphology of Apinagia multibranchiata (Podostemaceae) from the Venezuelan Guyanas. Bot J Linn Soc 132:299–323

    Article  Google Scholar 

  25. Jäger-Zürn I (1999) Morphology of Podostemaceae. V. Developmental morphology of the shoot system of Podostemum subulatum (Podostemaceae: Podostemoideae). Beitr Biol Pflanzen 71:281–334

    Google Scholar 

  26. Jäger-Zürn I (2000) Morphology of Podostemaceae. VI. Crustose root and root-born shoots of Zeylanidium olivaceum (Podostemaceae: Podostemoideae). Flora 195:61–82

    Google Scholar 

  27. Jäger-Zürn I (2002) Comparative studies in the morphology of Crenias weddelliana and Maferria indica with reference to Sphaerothylax abyssinica (Podostemaceae: Podostemoideae). Bot J Linn Soc 138:63–84

    Article  Google Scholar 

  28. Jäger-Zürn I (2005) Shoot apex and spathella: two problematical structures of Podostemaceae–Podostemoideae. Plant Syst Evol 253:209–218

    Article  Google Scholar 

  29. Imaichi R, Hiyama Y, Kato M (2005) Leaf development in absence of shoot apical meirstem in Zeylanidium subulatum (Podostemaceae). Ann Bot 96:51–58

    Article  PubMed  Google Scholar 

  30. Koi S, Imaichi R, Kato M (2005) Endogenous leaf initiation in the apical-meristemless shoot of Cladopus queenslandicus (Podostemaceae) and implications for evolution of shoot morphology. Int J Plant Sci 166:199–206

    Article  Google Scholar 

  31. Katayama N, Koi S, Kato M (2008) Developmental anatomy of the reproductive shoot in Hydrobryum japonicum (Podostemaceae). J Plant Res 121:417–427

    Article  PubMed  Google Scholar 

  32. Kita Y, Kato M (2001) Infrafamilial phylogeny of the aquatic angiosperm Podostemaceae inferred from the nucleotide sequences of the matK gene. Plant Biol 3:156–163

    Article  CAS  Google Scholar 

  33. Jäger-Zürn I (1970) Morphologie der Podostemaceae I. Tristicha trifaria (Bory ex Willd.) Spreng. Beitr Biol Pflanzen 47:11–52

    Google Scholar 

  34. Jäger-Zürn I (1992) Morphologie der Podostemaceae II. Indotristicha ramosissima (Wight) van Royen (Tristichoideae). Beitr Biol Pflanzen 80:1–48

    Google Scholar 

  35. Jäger-Zürn I (1997) Comparative morphology of the vegetative structures of Tristicha trifaria, Indotristicha ramosissima and Dalzellia ceylanica (Podostemaceae, Tristichoideae): a review. Aquat Bot 57:71–96

    Article  Google Scholar 

  36. Sharma BD, Karthikeyan S, Shetty BV (1974) Indotristicha tirunelveliana Sharma, Karthik. & Shetty—a new species of Podostemaceae from South India. Bull Bot Surv India 16:157–161

    Google Scholar 

  37. Cusset G, Cusset C (1988) Etude sur les Podostemales. 10. Structures florales et végétatives des Tristichaceae. Bull Mus Natl Hist Nat Sect B Adansonia Bot Phytochim 10:179–218

    Google Scholar 

  38. Rutishause R, Huber KA (1991) The developmental morphology of Indotristicha ramosissima (Podostemaceae, Tristichoideae). Plant Syst Evol 178:195–223

    Google Scholar 

  39. Imaichi R, Ichiba M, Kato M (1999) Developmental morphology and anatomy of the vegetative organs in Malaccotristicha malayana (Podostemaceae). Int J Plant Sci 160:253–259

    Article  Google Scholar 

  40. Koi S, Kato M (2007) Developmental morphology of shoot in Weddellina squamulosa (Podostemaceae) and implications for shoot evolution in the Podostemaceae. Ann Bot 99:1121–1130

    Article  PubMed  Google Scholar 

  41. Fujinami R, Imaichi R (2009) Developmental anatomy of Terniopsis malayana (Podostemaceae, subfamily Tristichoideae), with implications for body plan evolution. J Plant Res 122:551–558

    Article  PubMed  Google Scholar 

  42. 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 

  43. Brand U et al (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619

    Article  PubMed  CAS  Google Scholar 

  44. Schoof H et al (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:35–644

    Article  Google Scholar 

  45. Kieffer M et al (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573

    Article  PubMed  CAS  Google Scholar 

  46. Chen S-K et al (2009) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230:827–840

    Article  PubMed  CAS  Google Scholar 

  47. Liang D et al (2009) Molecular dissection of the pea shoot apical meristem. J Exp Bot 60:4201–4213

    Article  PubMed  CAS  Google Scholar 

  48. Stuurman J, Jäggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218

    Article  PubMed  CAS  Google Scholar 

  49. Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119:823–831

    Google Scholar 

  50. Long JA et al (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69

    Article  PubMed  CAS  Google Scholar 

  51. Long JA, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 218:341–353

    Article  PubMed  CAS  Google Scholar 

  52. Waites R et al (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 

  53. Timmermans MCP et al (1999) ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284:151–153

    Article  PubMed  CAS  Google Scholar 

  54. Tsiantis M et al (1999) The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284:154–156

    Article  PubMed  CAS  Google Scholar 

  55. Byrne ME et al (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–971

    Article  PubMed  CAS  Google Scholar 

  56. Ori N et al (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127:5523–5532

    PubMed  CAS  Google Scholar 

  57. Guo M et al (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58

    Article  PubMed  CAS  Google Scholar 

  58. Landolt E (1998) Anatomy of the Lemnaceae (duckweeds). In: Landolt E, Jäger-Zürn I, Schnell RAA (eds) Extreme adaptations in angiospermous hydrophytes. Gebrüder Borntraeger, Berlin

    Google Scholar 

  59. Lemon GD, Posluszny U (2000) Comparative shoot development and evolution in the Lemnaceae. Int J Plant Sci 161:733–748

    Article  Google Scholar 

  60. Jäger-Zürn I (1995) Morphologie der Podostemaceae. III. Dalzellia ceylanica (Gard.) Wight (Tristichoideae). Trop Subtrop Pflanzen 92:7–77

    Google Scholar 

  61. Jäger-Zürn I (2002) Morphology and morphogenesis of ensiform leaves in Apinagia multibranchiata and Mourera fluviatilis (Podostemaceae–Podostemoideae). Flora 197:394–407

    Article  Google Scholar 

  62. Jäger-Zürn I (2005) Structural analysis of the dissected ensiform leaves and shoot morphology of Marathrum foeniculaceum (Podostemaceae). Flora 200:229–244

    Article  Google Scholar 

  63. Hiyama Y, Tsukamoto I, Imaichi R et al (2002) Developmental anatomy and branching of roots of four Zeylanidium species (Podostemaceae), with implications for evolution of foliose roots. Ann Bot 90:735–744

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank M. Kato for his encouragement for the preparation of this paper and useful suggestions on the manuscript. We also thank H. Hirano, T. Suzaki, and T. Yamada for their technical advices, and T. Wongprasert, R. Imaichi, and R. Fujinami who helped us collect materials used by the studies cited in this paper. This study was supported by a Grant-in Aid for Scientific Research from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Satoshi Koi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this protocol

Cite this protocol

Koi, S., Katayama, N. (2013). Gene Expression Analysis of Aquatic Angiosperms Podostemaceae to Gain Insight into the Evolution of Their Enigmatic Morphology. In: De Smet, I. (eds) Plant Organogenesis. Methods in Molecular Biology, vol 959. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-221-6_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-62703-221-6_5

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-62703-220-9

  • Online ISBN: 978-1-62703-221-6

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics