Anatomical relations among endophytic holoparasitic angiosperms, autotrophic host plants and mycorrhizal fungi: A novel tripartite interaction

Abstract

Mycorrhizae are widespread mutualistic symbioses crucial for the functioning of terrestrial ecosystems. Not all plants associate with mycorrhizae; most parasitic plants have been suggested to be nonmycorrhizal because they have developed alternative strategies to obtain nutrients. In endophytic parasitic plants, whose vegetative bodies grow completely inside their mycorrhizal host roots, the opportunity for establishing a tripartite association seems evident, but information on these systems is lacking. In studying natural associations among the endophytic holoparasite Cytinus hypocistis, their Cistaceae host species, and associated mycorrhizal fungi, we found that mycorrhizae were associated with the hosts and the parasites, reaching high frequencies of colonization. In parasitic and host root tissues, mycorrhizal fungi spread in the parenchymatic cells by intracellular growth and formed hyphal coils and vesicles, while the cambium and the vascular tissues were never colonized. This report is the first on a tripartite association of an endophytic parasitic plant, its host, and mycorrhizae in natural conditions, representing a novel trophic interaction not previously reported within the angiosperms. Additional studies on the interactions occurring among these three players are needed because they may be crucial to our understanding of how this mutualistic-antagonistic system is functioning and evolving.

Commentary on the de Vega et al. (2010) paper on hyphae in the parasitic plant Cytinus: Mycorrhizal fungi growing within plants are not always mycorrhizal1

“…In conclusion, the endophytic and saprophytic capabilities of AM fungi have been well documented and are consistent with the observations presented by de Vega et al (2010) for Cytinus (e.g., Cázares and Trappe, 1993; DeMars and Boerner, 1996; Giovannetti and Sbrana, 1998; Brundrett, 2006). Unfortunately, the multifunctional nature of these fungi has created contradictions in the mycorrhizal literature, since fungi detected within roots of plants that are expected to be nonhosts have been interpreted as mycorrhizal associates in some cases and as endophytes in others (Brundrett, 2009).…”

“…The recent paper by de Vega et al (2010) contains some interesting observations about fungi within a parasitic plant and its host, which they interpret as a novel three‐way plant–plant–fungus association. However, their hypothesis is not conclusively supported by the data presented, and other interpretations of their observations are possible.…”

“…(7) A separate issue that also should be considered is that members of the Cistaceae normally are ectomycorrhizal as their primary association, but may also have AM (Malloch and Thorn, 1985; Comandini et al, 2006). Thus, the species sampled by de Vega et al (2010) are likely to have had ectomycorrhizal roots that were overlooked. It is common for AM fungi to grow as endophytes in ectomycorrhizal species (Cázares and Trappe, 1993), so these fungi may only have a minor role in the Cistaceae plants sampled.…”

Host-Parasite-Bacteria Triangle: The Microbiome of the Parasitic Weed Phelipanche aegyptiaca and Tomato-Solanum lycopersicum (Mill.) as a Host

“…Furthermore, since endophytic mycorrhizal fungi contain a large amount of bacteria in the ectomycorrhizal root tips (Sbrana et al, 2002), it might spread endophytic bacteria while colonizing the tomato. de Vega et al (2010) demonstrated tripartite association among a holoparasitic weed ( Cytinus ), its host Cistaceae species, and mycorrhizal fungi. However, studies on endophytic bacteria in parasitic weed have not been reported yet.…”

Biological Nitrogen Fixation: Importance, Associated Diversity, and Estimates

“…Nitrogen-fi xing bacteria, including rhizobia and mycorrhizal fungi, form mutualistic symbiotic associations with legumes. In this association, which is known as tripartite (Bonfante and Anca 2009 ;Vega et al 2010 ), the mycorrhizal mycelia through the network may increase the absorption and solubilization of phosphorus by translocating phosphorus in the soil to rhizobia located on plant nodules. Rhizobia fi x nitrogen and provide it in the form of ammonia to the plant, which, in turn, provides carbohydrate to microsymbionts (Silveira et al 2001 ;Gross et al 2004 ).…”