Abstract
Main conclusionSiderophores are a driver ofPinus sylvestrisroot responses to metabolites secreted by pathogenic and mycorrhizal fungi.Structurally different siderophores regulate the uptake of Fe by microorganisms and may play a key role in the colonization of plants by beneficial or pathogenic fungi. Siderophore action, however, may be dependent on the distribution of Fe within cells. Here, the involvement of siderophores in determining the changes of organelle morphology and element composition of some cellular fractions of root cells in Pinus sylvestris to trophically diverse fungi was investigated. Changes in the morphology and concentrations of different elements within organelles of root cells in response to three structurally different siderophores were examined by transmission electron microscopy combined with energy-dispersive X-ray spectroscopy. Weak development of mitochondrial cristae and the deposition of backup materials in plastids occurred in the absence of Fe in the structures of triacetylfusarinine C and ferricrocin. In response to metabolites of both pathogenic and mycorrhizal fungi, Fe accumulated mainly in the cell walls and cytoplasm. Fe counts increased in all of the analyzed organelles in response to applications of ferricrocin and triacetylfusarinine C. Chelation of Fe within the structure of siderophores prevents the binding of exogenous Fe, decreasing the abundance of Fe in the cell wall and cytoplasm. The concentrations of N, P, K, Ca, Mn, Cu, Mg, and Zn also increased in cells after applications of ferricrocin and triacetylfusarinine C, while the levels of these elements decreased in the cell wall and cytoplasm when Fe was present within the structure of the siderophores. These results provide insight into the siderophore-driven response of plants to various symbionts.
Highlights
The first stages of fungal entry into a plant host constitute a complex process regulated by numerous host defense responses, some of which are associated with Fe regulatoryElectronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.1 3 Vol.:(0123456789)Planta (2019) 249:1747–1760 establishing symbiosis, while plant hosts attempt to control Fe homeostasis to prevent fungal spread
When the host root cells were exposed to metabolites of F. oxysporum, several small osmophilic droplets were noticed within mitochondria and nuclei (Fig. 1b), while small vacuoles and vesicles with electron-dense material located in close vicinity to vacuole membrane were observed (Fig. 1c) in the case of H. crustuliniforme
Electron-dense deposits were frequently observed to be present within cell walls, which was not observed when an Fe-deprived form of ferrioxamine was used to treat the root cells (Fig. 1h)
Summary
The types of fungal siderophores that have been identified far include hydroxamate-type ones, which range in complexity from monomers, dimers, and trimers to cyclic forms that are classified into three structural families: fusarinines, coprogens, and ferrichromes (Renshaw et al 2002) The trimer forms, such as triacetylfusarinine C, have greater potential to affect plant susceptibility to Fusarium infection (Brown et al 2017). The function of siderophores may be associated with both their ability to scavenge Fe and their Fe-binding strength, which are dictated by their structure (Miethke and Marahiel 2007; Dellagi et al 2009; Aznar et al 2014) This raises the question of how the Fe affinity of different siderophores and their overall structure may affect the nature of a plant–fungus interaction
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