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To attract or to repel? Diversity, evolution and role of the “most peculiar organ” in the Cuscuta flower (dodder, Convolvulaceae)—the infrastaminal scales

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Abstract

Cuscuta (dodders) is the only genus in Convolvulaceae and the Solanales more broadly in which corolla-stamen structures called infrastaminal scales (IFS) have reached a high degree of elaboration and diversification in a great number of species. Historically, morphological diversity of IFS has provided some of the most useful taxonomic characters at the species-level. However, their function has not been determined. We have performed a comparative study of the IFS in 147 Cuscuta taxa using light, scanning and transmission electron microscopy, and results were analyzed in relation to a Cuscuta phylogeny obtained from a combined analysis of nuclear ITS and plastid trnL-F sequences. The morphology and histochemistry of scales and/or trichomes on the staminal filaments were also examined in several other Convolvulaceae genera to provide a preliminary foundation for homology interpretation. To test the hypothesis that the role of IFS in Cuscuta is connected to sexual reproduction, we analyzed the correlations between scale characters and previously published values for pollen/ovule ratios and the number of stomata found in the nectary at the base of the ovary. While the correlations at the level of the entire genus were very low, subgeneric partitions revealed a strong relationship between scale characters and sexual reproduction indicators in subgenus Monogynella. However, this connection declined drastically in the subgenera Cuscuta and Grammica. Our results strongly suggest that scales in Cuscuta evolved in connection to a modification of their function in the flower: from nectar protection and holding in the first diverged subgenus Monogynella, to ovary/ovule protection against herbivorous insects in the derived subgenera Cuscuta and Grammica. Thus at least in the case of the latter subgenera, the protective/repellent role of the IFS may conflict with the attractant/rewarding function of the nectary found at the base of the ovary. In subgenus Monogynella, IFS fimbriae are similar to uniseriate glandular hairs, with the secretory cells entirely exposed. In the subgenera Grammica and Cuscuta, the fimbriae become more complex, with an internal distal laticifer, and a precise mechanism of latex release. Our study elaborates further on the development and ultrastructure of scales in C. gronovii, and provides details on the anatomy of the IFS in other species. The new morphology and micromorphology data confirm the significance of these structures for species-level systematics.

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Acknowledgments

We would like to thank Andrew McLean and Nicole Atcheson for their help with floral dissections. Susan Belfry was a tremendous help with technical assistance for TEM. We are also grateful to Peter Endress and Gerhard Prenner for great suggestions that improved an earlier version of this article. Tom Van Devender, Ignacio García Ruiz, Eleazar Carranza, and the following herbaria provided the plant material: AAU, ALTA, ARIZ, ASU, B, BAB, BOL, BRIT, CANB, CAS, CEN, CHR, CHSC, CIIDIR, CIMI, CTES, DAO, F, G, GH, H, HUFU, IAC, IEB, IND, J, JEPS, LL, LP, LPB, LPS, K, MEL, MERL, MEXU, MICH, MO, NMC, NY, OAC, OKLA, OSC, OXF, PACA, PRE, QCNE, QFA, P, PACA, RB, RSA, SAM, S, SD, SGO, SI, SPF, TEX, TRT, TRTE, UA, UB, UBC, UCR, UCT, UNB, UNM, UPRRP, UPS, US, USAS, WTU and XAL. This research was supported by a Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery grant to M. Costea (327013-12), an undergraduate NSERC Grant to K. Dockstader (2011–2012), and an undergraduate WLU FOSSA grant to C. Clayson.

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  1. Department of Biology, Wilfrid Laurier University, Waterloo, ON, N2T1H8, Canada

    Stephanie Riviere, Courtney Clayson, Kristy Dockstader & Mihai Costea

  2. Department of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, L5L1C6, Canada

    Michael A. R. Wright

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  1. Stephanie Riviere
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Riviere, S., Clayson, C., Dockstader, K. et al. To attract or to repel? Diversity, evolution and role of the “most peculiar organ” in the Cuscuta flower (dodder, Convolvulaceae)—the infrastaminal scales. Plant Syst Evol 299, 529–552 (2013). https://doi.org/10.1007/s00606-012-0741-2

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