Abstract
Peltate leaf architecture has evolved from conventional bifacial leaves many times in flowering plant evolution. Characteristics of peltate leaves, such as the differentiation of a cross zone and of a radially symmetric, margin-less petiole, have also been observed in mutants of genes responsible for adaxial-abaxial polarity establishment. This suggests that altered regulation of such genes provided a mechanism for the evolution of peltate leaf structure. Here, we show that evolution of leaf peltation in Tropaeolum majus, a species distantly related to Arabidopsis thaliana, was associated with altered expression of Tropaeolum majus FILAMENTOUS FLOWER (TmFIL), a gene conferring abaxial identity. In situ hybridization indicates that adaxial and abaxial domains are established in early leaf primordia as in species with bifacial leaves. Upon initiation of the cross zone by fusion of the blade margins, localized expansion of TmFIL to the upper leaf side could be seen, indicating a local loss of adaxial leaf identity. The observed changes in expression are consistent with a role of TmFIL in radialization of the petiole and circularization of the leaf blade margin by the cross zone. In addition, expression was observed in segment primordia and during expansion of the bifacial blade, suggesting additional roles for TmFIL in leaf development.
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References
Busch A, Gleissberg S (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217:841–848
Ebel F (1998) Die Schildblättrigkeit krautiger Angiospermen-Sippen in ihrer Beziehung zu Standort und Verbreitung. Flora 193:203–224
Engstrom EM, Izhaki A, Bowman JL (2004) Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiol 135:685–694
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
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002
Gleissberg S (2004) Comparative analysis of leaf shape development in Eschscholzia californica and other Papaveraceae-Eschscholzioideae. Am J Bot 91:306–312
Gleissberg S, Kim M, Jernstedt J, Sinha N (1999) The regulation of dorsiventral symmetry in plants. In: Kato M (ed) Biology of biodiversity. Springer Verlag, Berlin Heidelberg New York, pp 223–241
Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst Evol 199:121–152
Jang S, Hur J, Kim S-J, Han M-J, Kim S-R, An G (2004) Ectopic expression of OsYAB1 causes extra stamens and carpels in rice. Plant Mol Biol 56:133–143
Kim M, McCormick S, Timmermans M, Sinha N (2003a) The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424:438–443
Kim M, Pham T, Hamidi A, McCormick S, Kuzoff RK, Sinha N (2003b) Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130:4405–4415
Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481
McConnell JR, Barton MK (1995) Effects of mutations in the PINHEAD gene of Arabidopsis on the formation of shoot apical meristems. Dev Genet 16:358–366
McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942
Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family are required to establish polarity in lateral organs. Development 126:4117–4128
Swofford DL (2001) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, Mass.
Waites R, Hudson A (1995) Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154
Watanabe K, Okada K (2003) Two discrete cis elements control the abaxial side-specific expression of the FILAMENTOUS FLOWER gene in Arabidopsis. Plant Cell 15:2592–2602
Xu L, Xu Y, Dong A, Sun Y, Pi L, Xu Y, Huang H (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097–4107
Zachgo S (2002) In situ hybridization. In: Gilmartin PM, Bowler C (eds) Molecular plant biology, vol. 2. Oxford University Press, Oxford, UK, pp 41–63
Acknowledgements
We thank J. Bowman (Davis, USA) for initial hints on oligo design and Yuval Eshed (Rehovot, Israel) and an anonymous reviewer for suggestions. This work was funded by grants from the B3 program and the Forschungsfonds at the University of Mainz to S.G.
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Gleissberg, S., Groot, E.P., Schmalz, M. et al. Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev Genes Evol 215, 313–319 (2005). https://doi.org/10.1007/s00427-005-0479-8
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DOI: https://doi.org/10.1007/s00427-005-0479-8