A living bridge between two enemies: haustorium structure and evolution across parasitic flowering plants

Abstract

Parasitic flowering plants are characterized by the development of an organ known as haustorium, which has evolved in multiple independent angiosperms clades. The haustorium has also been deemed “the most plastic of organs” due to its ability to accommodate physiological and anatomical differences between the parasite itself and its host plants. This is achieved through the development of vascular connections, which involve the differentiation of various specialized cell types by the parasite. The development, structure, and evolution of the haustorium and the connections it fosters are reviewed here considering all 12 parasitic plant lineages. A multi-level comparison between “model” parasitic plants, such as Orobanchaceae and Cuscuta species, with members of often neglected groups, such as Lennoaceae, Mitrastemonaceae, and Santalales yields the idea of a shared general body plan of the mature haustorium. This proposed haustorium bauplan is composed of an upper part, including structures associated with mechanical attachment to the host body, and a lower part, including all parasitic tissues and cell types within the host body. The analysis of multi-level convergence is also applied here to the comparison between haustoria and other plant organs. Considering the structure, molecular development, and functionality of this organ under the framework of continuum and process plant morphology, I propose the interpretation of haustoria as morphological misfits.

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Fig. 1

modified from Nickrent 2020) indicating 12 independent origins of the parasitic lifestyle (in red). b Pyrularia pubera Michx. (Santalaceae, Santalales), a root hemiparasitic tree. c Lennoa madreporoides Lex. (Lennoaceae), a root holoparasite. d Castilleja mexicana (Hemsl.) A. Gray (Orobanchaceae), a root hemiparasitic herb. e Cuscuta campestris Yunck. (Convolvulaceae), a parasitic vine. f Phoradendron juniperinum Engelm. ex A. Gray (Santalaceae), a mistletoe. g Mitrastemon matudae Yamam. (Mitrastemonaceae), an endoparasite. p parasite, h host

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Acknowledgements

I would like to thank Dr. Gregorio Ceccantini for the support, mentoring, and fruitful discussions during many years of learning and collaborations. Dr. Fernanda Oliveira provided valuable suggestions to earlier versions of this work. Dr. Rafael Cruz provided excellent discussions about evolutionary developmental biology, identity of plant organs, and morphological misfits. I am also thankful to colleagues Dr. Charles Davis and Dr. Maximilian Weigend who kindly provided some of the photographs used in this work. The image used in Fig. 2g is under a Creative Commons, Non-Commercial Share-Alike 3.0 type of license (https://creativecommons.org/licenses/by-nc-sa/3.0/legalcode). I also thank the Harvard University Herbaria of Harvard University for allowing the capturing of images from specimens in the anatomical slide collection (Fig. 6a–h). Funding was provided by the Harvard University Herbaria.

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Teixeira-Costa, L. A living bridge between two enemies: haustorium structure and evolution across parasitic flowering plants. Braz. J. Bot 44, 165–178 (2021). https://doi.org/10.1007/s40415-021-00704-0

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Keywords

  • Body plan
  • Continuum morphology
  • Morphological evolution
  • Orobanchaceae
  • Rafflesiaceae
  • Santalales