Plant Growth Regulation

, Volume 72, Issue 2, pp 123–140 | Cite as

GA2 and GA20-oxidase expressions are associated with the meristem position in Streptocarpus rexii (Gesneriaceae)

  • Kanae Nishii
  • Meng-Jung Ho
  • Yen-Wei Chou
  • Damiano Gabotti
  • Chun-Neng Wang
  • Alberto Spada
  • Michael Möller
Original paper


We examined genes involved in the regulatory pathway of gibberellin (GA) in meristems of Streptocarpus rexii. The plants do not possess a typical shoot apical meristem (SAM) and form unique meristems: the basal meristem extends the lamina area of one cotyledon to produce anisocotylous seedlings; the groove meristem forms new leaves at the base of the macrocotyledon. Exogenous application of GA significantly suppresses the basal meristem activity in developing cotyledons and the seedlings remain isocotyl. To examine the role of endogenous GA on these meristems in vivo, we isolated homologs of GA2-oxidase responsible for degrading active GAs (SrGA2ox), and GA20-oxidase regulating the rate limiting step of active GA synthesis (SrGA20ox). During embryogenesis, while first partly overlapping, the expression of SrGA2ox and SrGA20ox became more differentiated and mutually exclusive, ending with SrGA2ox being expressed solely in the adaxial–proximal domain of the embryo in regions with meristem activity, whereas SrGA20ox was restricted to the fork between the two cotyledons. The latter may be responsible for suppressing the formation of an embryonic SAM in S. rexii. In developing seedlings, SrGA2ox expression also followed the centers of meristem activity, where SrGA20ox expression was excluded. Our results suggest that low levels of GA are required in S. rexii meristems for their establishment and maintenance. Thus, the meristems in S. rexii share similar regulatory pathways suggested for the SAM in model plants, but that in S. rexii evolutionary modifications involving a lateral transfer of function, from shoot to leaves, is implicated in attaining the unusual morphology of the plants.


Basal meristem Gibberellin20-oxidase Gibberellin2-oxidase Gibberellins Macrocotyledon Streptocarpus 



This work was supported, in part, by a Taiwan-Italy Scientific Research Cooperation grant from the National Science Council (NSC) in Taiwan and National Research Council (CNR) in Italy (Grant Number 99-2923-B-002-007-MY2) and the Excellent Research Program from the National Taiwan University (10R30701, NTU) to CW. KN is supported by the NSC funding NSC 101-2811-B-002-150 and Sibbald Trust at Royal Botanic Garden Edinburgh (UK). We thank Dr. Min-Liang Kuo (NTU), Dr. Shin-Tong Jeng (NTU), Dr Tsan-Piao Lin (NTU) and Dr. Shih-Ying Hwang (National Taiwan Normal University, Taiwan) for their research funding support and helpful comments on this study. We thank Dr. K.-J. Tang and Ms. Y.-Y. Gao (TechComm, NTU) for technical support and enabling access to real-time PCR facilities. We thank the Science Division of RBGE for supporting this work. RBGE is supported by the Rural and Environment Science and Analytical Services division (RESAS) in the Scottish Government.

Supplementary material

10725_2013_9844_MOESM1_ESM.doc (27 kb)
Supplementary material 1 (DOC 27 kb)
10725_2013_9844_MOESM2_ESM.ppt (3.1 mb)
Supplementary material 2 (PPT 3176 kb)


  1. Bolduc N, Hake S (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21:1647–1658PubMedCentralPubMedCrossRefGoogle Scholar
  2. Burtt BL (1970) Studies in Genseriaceae of the old world XXXI: some aspect of functional evolution. Notes R Bot Gard Edinb 30:1–10Google Scholar
  3. Carzoli FG, Michelotti V, Fambrini M, Salvini M, Pugliesi C (2009) Molecular cloning and organ-specific expression of two Gibberellin 20-oxidase genes of Helianthus annuus. Plant Mol Biol Rep 27:144–152CrossRefGoogle Scholar
  4. Cutler DF, Botha T, Stevenson DW (2007) Plant anatomy: an applied approach. Blackwell Publishing, OxfordGoogle Scholar
  5. Frisse A, Pimenta MJ, Lange T (2003) Expression studies of gibberellin oxidases in developing pumpkin seeds. Plant Physiol 131:1220–1227PubMedCentralPubMedCrossRefGoogle Scholar
  6. Hake S, Smith HMS, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of KNOX genes in plant development. Annu Rev Cell Dev Biol 20:125–151PubMedCrossRefGoogle Scholar
  7. Harrison J, Möller M, Langdale J, Cronk Q, Hudson A (2005) The role of KNOX genes in the evolution of morphological novelty in Streptocarpus. Plant Cell 17:430–443PubMedCentralPubMedCrossRefGoogle Scholar
  8. Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565PubMedCrossRefGoogle Scholar
  9. Hayashi T, Polonenko DR, Camirand A, Maclachlan G (1986) Pea xyloglucan and cellulose IV. Assembly of ß-glucans by pea protoplasts. Plant Physiol 82:301–306PubMedCentralPubMedCrossRefGoogle Scholar
  10. Imaichi R, Nagumo S, Kato M (2000) Ontogenetic anatomy of Streptocarpus grandis (Gesneriaceae) with implications for evolution of monophylly. Ann Bot 86:37–46CrossRefGoogle Scholar
  11. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565PubMedCrossRefGoogle Scholar
  12. Jong K (1970) Developmental aspects of vegetative morphology of Streptocarpus. PhD dissertation, University of EdinburghGoogle Scholar
  13. Jong K, Burtt BL (1975) The evolution of morphological novelty exemplified in the growth patterns of some Gesneriaceae. New Phytol 75:297–311CrossRefGoogle Scholar
  14. Jürgens G (2001) Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J 20:3609–3616PubMedCrossRefGoogle Scholar
  15. Kuwabara A, Nagata T (2006) Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae). Planta 224:761–770PubMedCrossRefGoogle Scholar
  16. Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, Whiteway M (2010) Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8:e1000329PubMedCentralPubMedCrossRefGoogle Scholar
  17. Lee DJ, Zeevaart JAD (2005) Molecular cloning of GA 2-Oxidase3 from spinach and its ectopic expression in Nicotiana sylvestris. Plant Physiol 138:243–254PubMedCentralPubMedCrossRefGoogle Scholar
  18. Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69PubMedCrossRefGoogle Scholar
  19. Mantegazza R, Möller M, Harrison CJ, Fior S, De Luca C, Spada A (2007) Anisocotyly and meristem initiation in an unorthodox plant, Streptocarpus rexii (Gesneriaceae). Planta 225:653–663PubMedCrossRefGoogle Scholar
  20. Mantegazza R, Tononi P, Möller M, Spada A (2009) WUS and STM homologs are linked to the expression of lateral dominance in the acaulescent Streptocarpus rexii (Gesneriaceae). Planta 230:529–542PubMedCrossRefGoogle Scholar
  21. Nishii K, Nagata T (2007) Developmental analyses of the phyllomorph formation in the rosulate species Streptocarpus rexii (Gesneriaceae). Plant Syst Evol 265:135–145CrossRefGoogle Scholar
  22. Nishii K, Kuwabara A, Nagata T (2004) Characterization of anisocotylous leaf formation in Streptocarpus wendlandii (Gesneriaceae): significance of plant growth regulators. Ann Bot 94:457–467PubMedCrossRefGoogle Scholar
  23. Nishii K, Möller M, Kidner CA, Spada A, Mantegazza R, Wang C-N, Nagata T (2010) A complex case of simple leaves: indeterminate leaves co-express ARP and KNOX1 genes. Dev Gen Evol 220:25–40CrossRefGoogle Scholar
  24. Nishii K, Wang C-N, Spada A, Nagata T, Möller M (2012) Gibberellin as a suppressor of lateral dominance and inducer of apical growth in the unifoliate Streptocarpus wendlandii (Gesneriaceae). N Z J Bot 50:267–287CrossRefGoogle Scholar
  25. Ochman H, Gerber AS, Hart DL (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120:621–623PubMedGoogle Scholar
  26. Olszewski N, Sun T-P, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80PubMedCentralPubMedGoogle Scholar
  27. Park S, Harada JJ (2008) Arabidopsis embryogenesis. Methods Mol Biol 427:3–16PubMedCrossRefGoogle Scholar
  28. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:E36PubMedCentralPubMedCrossRefGoogle Scholar
  29. Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Benlloch R, Nilsson O, Thomas SG, Hedden P, Phillipsa AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20:2420–2436PubMedCentralPubMedCrossRefGoogle Scholar
  30. Rosenblum IM, Basile DV (1984) Hormonal-regulation of morphogenesis in Streptocarpus and its relevance to evolutionary history of the Gesneriaceae. Am J Bot 71:52–64CrossRefGoogle Scholar
  31. Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001a) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590PubMedCrossRefGoogle Scholar
  32. Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H, Iwahori S, Matsuoka M (2001b) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516PubMedCentralPubMedCrossRefGoogle Scholar
  33. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675PubMedCrossRefGoogle Scholar
  34. Solfanelli C, Ceron F, Paolicchi F, Giorgetti L, Geri C, Ceccarelli N, Kamiya Y, Picciarelli P (2005) Expression of two genes encoding gibberellin 2- and 3-oxidases in developing seeds of Phaseolus coccineus. Plant Cell Physiol 46:1116–1124PubMedCrossRefGoogle Scholar
  35. Staheli JP, Boyce R, Kovarik D, Rose TM (2011) CODEHOP PCR and CODEHOP PCR primer design. In: Park DJ (ed) PCR protocols (Methods in molecular biology), vol 687. Humana Press, New York, pp 57–73Google Scholar
  36. Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, New YorkCrossRefGoogle Scholar
  37. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  38. Tanaka-Ueguchi M, Itoh H, Oyama N, Koshioka M, Matsuoka M (1998) Over-expression of tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J 15:391–400PubMedCrossRefGoogle Scholar
  39. Thomas SG, Phillips AL, Heddem P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci USA 96:4698–4703PubMedCrossRefGoogle Scholar
  40. Tononi P, Möller M, Bencivenga S, Spada A (2010) GRAMINIFOLIA homolog expression in Streptocarpus rexii is associated with the basal meristems in phyllomorphs, a morphological novelty in Gesneriaceae. Evol Dev 12:61–73PubMedCrossRefGoogle Scholar
  41. Veit B (2004) Determination of cell fate in apical meristems. Curr Opin Plant Biol 7:57–64PubMedCrossRefGoogle Scholar
  42. Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16:1206–1219PubMedCentralPubMedCrossRefGoogle Scholar
  43. Xu Y-L, Li L, Wu K, Peeters AJM, Gage DA, Zeevaart JAD (1995) The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: molecular cloning and functional expression. Proc Natl Acad Sci USA 92:6640–6644PubMedCrossRefGoogle Scholar
  44. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Life Science, Institute of Ecology and Evolutionary BiologyNational Taiwan UniversityTaipeiTaiwan
  2. 2.Royal Botanic Garden EdinburghEdinburghScotland, UK
  3. 3.Milan University Dipartimento Scienze Agrarie e Ambientali Territorio e AgroenergiaUniversità degli Studi di MilanoMilanItaly

Personalised recommendations