Striking developmental convergence in angiosperm endoparasites

Abstract

Plant parasitism has evolved 12 times within flowering plants (Nickrent, 2020). This phylogenetic diversity is accompanied by a wide variety of habits, geographical distribution, host preferences, morphologies, and developmental patterns (Kuijt, 1969;Heide-Jørgensen, 2008). A broad spectrum of photosynthetic capabilities is also represented among these plants, ranging from species fully capable of photosynthesis, to those that are achlorophyllous during all or most of their life cycle, thus rendering them entirely reliant on host resources (Bromham et al., 2013). A subset of plants in the latter category exhibits a particularly extreme degree of reduction: their vegetative body is reduced to mycelium-like filaments of parenchyma cells embedded within their host tissues. In these cases, the parasite only becomes visible during reproduction when the flower/inflorescence temporarily emerges from its host (Mauseth, 1990;Meijer and Veldkamp, 1993;Nikolov et al., 2014b). Due to this extremely reduced growth form, restricted to life inside its host, these plants are commonly referred to as endoparasites.This highly modified and cryptic growth habit has been best described in detail from a small number of mistletoe species (Těšitel, 2016). Mistletoes are widely distributed parasitic plants known as keystone species in both natural and human-altered ecosystems (

Endoparasitic plants and fungi show evolutionary convergence across phylogenetic divisions

“…In the past two decades, refreshed assessments of endoparasitic plant anatomy have progressed our understanding of the parasite–host interface (de Vega et al ., 2007; Amaral & Ceccantini, 2011; Nikolov et al ., 2014a; Nikolov & Davis, 2017). However, a comparative analysis of the anatomy and development of the four independent endoparasitic plant lineages was achieved only recently (Teixeira‐Costa et al ., 2021). This work demonstrates that species in the four exclusively endoparasitic families, the Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae, show a remarkably similar developmental trajectory.…”

“…Astonishingly, in the Rafflesiaceae, the endophyte appears to develop directly from a proembryo, like within the Orchidaceae, rather than an embryo proper (Nikolov et al ., 2014a). In all four endoparasitic lineages, differentiation of vascular cells is only detected among endophyte cells once flower bud formation begins (Teixeira‐Costa et al ., 2021). At this stage, substantial alterations to the host xylem micromorphology occur.…”

“…Cytinus and Pilostyles also trigger massive distortions of their host tissues when the flowering shoot emerges from the continuous sheath of the endophyte (de Vega et al ., 2007; Amaral & Ceccantini, 2011). Indeed, distortion of host tissue is common across endoparasitic lineages, characterized by the differentiation of new vessel elements towards the parasite flower or inflorescence (Teixeira‐Costa et al ., 2021). Given the convergent life history of plant and fungal endophytes, interesting parallels may also be drawn with the emergence of fungal fruiting bodies from their hosts.…”

“…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). The endophyte can grow extensively throughout the host, even upwards to 13 m (Barkman et al ., 2017).…”

“…The endophyte can grow extensively throughout the host, even upwards to 13 m (Barkman et al ., 2017). Its cell filaments often anastomose to form extensive pockets of parasitic tissue in the host cortex and bark from which ‘sinkers’ then penetrate the host’s vascular tissue (Watanabe, 1933; Teixeira‐Costa 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).…”