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Duplicated STM-like KNOX I genes act in floral meristem activity in Eschscholzia californica (Papaveraceae)

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Abstract

In angiosperms, the shoot apical meristem is at the origin of leaves and stems and is eventually transformed into the floral meristem. Class I knotted-like homeobox (KNOX I) genes are known as crucial regulators of shoot meristem formation and maintenance. KNOX I genes maintain the undifferentiated state of the apical meristem and are locally downregulated upon leaf initiation. In Arabidopsis, KNOX I genes, especially SHOOTMERISTEMLESS (STM), have been shown to regulate flower development and the formation of carpels. We investigated the role of STM-like genes in the reproductive development of Eschscholzia californica, to learn more about the evolution of KNOX I gene function in basal eudicots. We identified two orthologs of STM in Eschscholzia, EcSTM1 and EcSTM2, which are predominantly expressed in floral tissues. In contrast, a KNAT1/BP-like and a KNAT2/6-like KNOX I gene are mainly expressed in vegetative organs. Virus-induced gene silencing (VIGS) was used to knockdown gene expression, revealing that both EcSTM genes are required for the formation of reproductive organs. Silencing of EcSTM1 resulted in the loss of the gynoecium and a reduced number of stamens. EcSTM2-VIGS flowers had reduced and defective gynoecia and a stronger reduction in the number of stamen than observed in EcSTM1-VIGS. Co-silencing of both genes led to more pronounced phenotypes. In addition, silencing of EcSTM2 alone or together with EcSTM1 resulted in altered patterns of internodal elongation and sometimes in other floral defects. Our data suggest that some aspects of STM function present in Arabidopsis evolved already before the basal eudicots diverged from core eudicots.

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Acknowledgments

S. Gleissberg received funding from the German Research Foundation (DFG) and a start-up fund from Ohio University. A. Becker received follow-up funding from the German Research Foundation (DFG). We thank N. Sinha (Davis) for providing sequences, Andrea Scholz (Mainz) for cloning of pTRV2-EcSTM1-b, Chi Elsie Zhang (Athens) for database work, Angelika Trambacz, and Werner Vogel (Bremen) for plant care, Friederike Koenig (Bremen) for discussions, Abdinasir Mohamud and Timothy Pritchard (Athens) for help with phenotypic scoring, and two anonymous reviewers for comments.

Author contributions

S. Gleissberg designed the project and led the research with A. Becker. S. Meyer cloned and characterized the genes with B. Townsley. Angelika Stammler contributed to cloning, carried out RT-PCR profiling, and performed the VIGS experiments with phenotypic scoring, data analyses, and data presentation. S. Gleissberg contributed to data analyses and presentation. A. Plant performed the phylogenetic analyses. A. Stammler, S. Gleissberg, and A. Becker wrote the manuscript.

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Authors and Affiliations

  1. Department of Environmental and Plant Biology, Ohio University, Porter Hall 500, Athens, OH, 45701, USA

    Angelika Stammler, Alastair R. Plant & Stefan Gleissberg

  2. Institute of Anatomy and Cell Biology, Justus-Liebig-University Giessen, Aulweg 123, 35392, Giessen, Germany

    Angelika Stammler

  3. Institut für Spezielle Botanik, Johannes Gutenberg-University Mainz, 55099, Mainz, Germany

    Sandra S. Meyer

  4. Department of Plant Biology, University of California Davis, 1002 Life Science, One Shields Ave, Davis, CA, 95616, USA

    Brad T. Townsley

  5. Evolutionary Developmental Genetics Group, University of Bremen, Leobener Str., UFT, 28139, Bremen, Germany

    Angelika Stammler & Annette Becker

  6. Evolutionary Developmental Genetics Group, Justus-Liebig-University Giessen, Heinrich-Buff-Ring 38, 35392, Giessen, Germany

    Annette Becker

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  1. Angelika Stammler
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  2. Sandra S. Meyer
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  3. Alastair R. Plant
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  4. Brad T. Townsley
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  5. Annette Becker
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  6. Stefan Gleissberg
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Correspondence to Stefan Gleissberg.

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Communicated by Sureshkumar Balasubramanian

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Stammler, A., Meyer, S.S., Plant, A.R. et al. Duplicated STM-like KNOX I genes act in floral meristem activity in Eschscholzia californica (Papaveraceae). Dev Genes Evol 223, 289–301 (2013). https://doi.org/10.1007/s00427-013-0446-8

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