The Enigma of Interspecific Plasmodesmata: Insight From Parasitic Plants.

Karsten Fischer,Maria Mulisch,Stian Olsen,Kirsten Krause,Lena Anna-Maria Lachner

doi:10.3389/fpls.2021.641924

Karsten Fischer, Maria Mulisch + Show 3 more

Open Access

https://doi.org/10.3389/fpls.2021.641924

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Abstract

Parasitic plants live in intimate physical connection with other plants serving as their hosts. These host plants provide the inorganic and organic compounds that the parasites need for their propagation. The uptake of the macromolecular compounds happens through symplasmic connections in the form of plasmodesmata. In contrast to regular plasmodesmata, which connect genetically identical cells of an individual plant, the plasmodesmata that connect the cells of host and parasite join separate individuals belonging to different species and are therefore termed “interspecific”. The existence of such interspecific plasmodesmata was deduced either indirectly using molecular approaches or observed directly by ultrastructural analyses. Most of this evidence concerns shoot parasitic Cuscuta species and root parasitic Orobanchaceae, which can both infect a large range of phylogenetically distant hosts. The existence of an interspecific chimeric symplast is both striking and unique and, with exceptions being observed in closely related grafted plants, exist only in these parasitic relationships. Considering the recent technical advances and upcoming tools for analyzing parasitic plants, interspecific plasmodesmata in parasite/host connections are a promising system for studying secondary plasmodesmata. For open questions like how their formation is induced, how their positioning is controlled and if they are initiated by one or both bordering cells simultaneously, the parasite/host interface with two adjacent distinguishable genetic systems provides valuable advantages. We summarize here what is known about interspecific plasmodesmata between parasitic plants and their hosts and discuss the potential of the intriguing parasite/host system for deepening our insight into plasmodesmatal structure, function, and development.

Highlights

Symplasmic domains are operational units which are formed by joining the protoplasts of cells by way of plasmodesmata (PD) that form complex structures across the plant cell walls (Ehlers and Kollmann, 2001) or by sieve pores that originate from PD (Kalmbach and Helariutta, 2019) but are limited to the sieve elements of the phloem
In Scenario 4, the parasite cell wall enzymes are secreted in a location where a pre-infection host PD is present
Young hyphae were often found to be surrounded by host cell walls that were stretched extremely thin [Figures 1D,E and Vaughn (2003)]. This provided evidence for extensive deconstruction and loosening of the host cell walls at the site of contact, but it remains speculative whether this thinning is mediated by host or parasite enzymes

Summary

Introduction

Symplasmic domains are operational units which are formed by joining the protoplasts of cells by way of plasmodesmata (PD) that form complex structures across the plant cell walls (Ehlers and Kollmann, 2001) or by sieve pores that originate from PD (Kalmbach and Helariutta, 2019) but are limited to the sieve elements of the phloem. Chimeric cell walls and symplasmic connections between the different hyphae and the host tissue provide cohesion between the partners and it is tempting to assume that they ensure the efficiency in nutrient uptake that the parasite depends on. A nice demonstration of macromolecular transport between host plants and Cuscuta and, with it, unequivocal proof for a continuous and efficient connection between parasite and host vascular bundles was provided using the green fluorescent protein (GFP) (Haupt et al, 2001; Birschwilks et al, 2007).

Results

Conclusion