Parasites on parasites: hyper-, epi-, and autoparasitism among flowering plants

Yuliya Krasylenko, Jakub Těšitel, Gregorio Ceccantini, Mariana Oliveira-da-Silva, Václav Dvořák, Daniel Steele, Yevhen Sosnovsky, Renata Piwowarczyk, David M. Watson, Luiza Teixeira-Costa

Onderzoeksoutput: Articlepeer review

15 Citaten (Scopus)

Samenvatting

All organisms engage in parasitic relations, as either parasites or hosts. Some species may even play both roles simultaneously. Among flowering plants, the most widespread form of parasitism is characterized by the development of an intrusive organ called the haustorium, which absorbs water and nutrients from the host. Despite this functionally unifying feature of parasitic plants, haustoria are not homologous structures; they have evolved 12 times independently. These plants represent ca. 1% of all extant flowering species and show a wide diversity of life histories. A great variety of plants may also serve as hosts, including other parasitic plants. This phenomenon of parasitic exploitation of another parasite, broadly known as hyper- or epiparasitism, is well described among bacteria, fungi, and animals, but remains poorly understood among plants. Here, we review empirical evidence of plant hyperparasitism, including variations of self-parasitism, discuss the diversity and ecological importance of these interactions, and suggest possible evolutionary mechanisms. Hyperparasitism may provide benefits in terms of improved nutrition and enhanced host–parasite compatibility if partners are related. Different forms of self-parasitism may facilitate nutrient sharing among and within parasitic plant individuals, while also offering potential for the evolution of hyperparasitism. Cases of hyperparasitic interactions between parasitic plants may affect the ecology of individual species and modulate their ecosystem impacts. Parasitic plant phenology and disperser feeding behavior are considered to play a major role in the occurrence of hyperparasitism, especially among mistletoes. There is also potential for hyperparasites to act as biological control agents of invasive primary parasitic host species.

Originele taal-2English
Pagina's (van-tot)8-21
Aantal pagina's14
TijdschriftAmerican Journal of Botany
Volume108
Nummer van het tijdschrift1
DOI's
StatusPublished - jan 2021

Bibliografische nota

Funding Information:
We thank staff of the Field Museum Herbarium and Harvard University Herbaria for allowing the use of photographed specimens in Fig. 2C and Fig. 2D and E, respectively. We also acknowledge the anonymous reviewers for their comments, which helped us expand on the discussion of the hyperparasitic phenomenon. Y.K. was supported by the European Regional Developmental Fund (project no. CZ.02.1.01/0.0/0.0/16_019/0000827). G.C. was supported by the São Paulo Research Foundation (FAPESP, grant 2012/22833-1). J.T. was supported by Czech Science Foundation (project no. 19-28491X). Y.S. was supported by Ivan Franko National University of Lviv (grant no. N/113-2003). R.P. was supported by the National Geographic Society (project no. GEFNE 192-16) and the Jan Kochanowski University (project no. SMGR.20.208-615). D.S. was supported by the University of California–Davis, Department of Plant Sciences research assistantship and the NSF funded Parasitic Plant Genome Project (IOS-1238057). L.T.C. was supported by a Harvard University Herbaria Research Fellowship. The authors declare that they have no conflict of interest.

Funding Information:
We thank staff of the Field Museum Herbarium and Harvard University Herbaria for allowing the use of photographed specimens in Fig. 2C and Fig. 2D and E , respectively. We also acknowledge the anonymous reviewers for their comments, which helped us expand on the discussion of the hyperparasitic phenomenon. Y.K. was supported by the European Regional Developmental Fund (project no. CZ.02.1.01/0.0/0.0/16_019/0000827). G.C. was supported by the São Paulo Research Foundation (FAPESP, grant 2012/22833‐1). J.T. was supported by Czech Science Foundation (project no. 19‐28491X). Y.S. was supported by Ivan Franko National University of Lviv (grant no. N/113‐2003). R.P. was supported by the National Geographic Society (project no. GEFNE 192‐16) and the Jan Kochanowski University (project no. SMGR.20.208‐615). D.S. was supported by the University of California–Davis, Department of Plant Sciences research assistantship and the NSF funded Parasitic Plant Genome Project (IOS‐1238057). L.T.C. was supported by a Harvard University Herbaria Research Fellowship. The authors declare that they have no conflict of interest.

Publisher Copyright:
© 2021 Botanical Society of America

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

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