Abstract
Endoparasitic plants are the most reduced flowering plants, spending most of their lives as a network of filaments within the tissues of their hosts. Despite their extraordinary life form, we know little about their biology. Research into a few species has revealed unexpected insights, such as the total loss of plastome, the reduction of the vegetative phase to a proembryonic stage, and elevated information exchange between host and parasite. To consolidate our understanding, we review life history, anatomy, and molecular genetics across the four independent lineages of endoparasitic plants. We highlight convergence across these clades and a striking trans-kingdom convergence in life history among endoparasitic plants and disparate lineages of fungi at the molecular and physiological levels. We hypothesize that parasitism of woody plants preselected for the endoparasitic life history, providing parasites a stable host environment and the necessary hydraulics to enable floral gigantism and/or high reproductive output. Finally, we propose a broader view of endoparasitic plants that connects research across disciplines, for example, pollen-pistil and graft incompatibility interactions and plant associations with various fungi. We shine a light on endoparasitic plants and their hosts as under-explored ecological microcosms ripe for identifying unexpected biological processes, interactions and evolutionary convergence.
Highlights
The most extreme holoparasites are the endoparasites – those that spend their entire life cycles within the tissues of other plants, except when briefly emerging to flower and set seed. These extraordinary plants are united by the production of an endophyte that composes undifferentiated cell filaments or cell masses embedded within the host, and a common developmental trajectory in which cell division leads to the formation of extensive parasitic tissue masses within their hosts’ cortex and bark tissues (Teixeira-Costa et al, 2021)
Our synthesis suggests that endoparasitic plants and their hosts are under-explored as living laboratories for identifying new and unexpected processes and interactions, and convergent evolution
The intimate association between plant and fungal pathogens has led to a high level of communication, for example the exchange of small RNAs (Weiberg et al, 2013; Wang & Dean, 2020) just as it has in endoparasitic plants
Summary
Parasitic plants have evolved at least 12 times from their free-living ancestors, constituting approximately 1.2% of flowering plant species (Nickrent, 2020). The most extreme holoparasites are the endoparasites – those that spend their entire life cycles within the tissues of other plants, except when briefly emerging to flower and set seed These extraordinary plants are united by the production of an endophyte that composes undifferentiated cell filaments or cell masses embedded within the host, and a common developmental trajectory in which cell division leads to the formation of extensive parasitic tissue masses within their hosts’ cortex and bark tissues (Teixeira-Costa et al, 2021). Its cell filaments often anastomose to form extensive pockets of parasitic tissue in the host cortex and bark from which ‘sinkers’ penetrate the host’s vascular tissue (Watanabe, 1933; TeixeiraCosta et al, 2021) These sinkers have been inferred to be analogous to roots, as they carry out a similar function of absorbing water and mineral nutrients (Amaral & Ceccantini, 2011). Our synthesis suggests that endoparasitic plants and their hosts are under-explored as living laboratories for identifying new and unexpected processes and interactions, and convergent evolution
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