Abstract
Arbuscular mycorrhizal (AM) symbiosis is one of the most prominent and beneficial plant–microbe interactions that facilitates mineral nutrition and confers tolerance to biotic and abiotic stresses. AM fungi colonize the root cortex and develop specialized structures called arbuscules where the nutrient exchange takes place. Arbuscule development is a highly controlled and coordinated process requiring the involvement of many plant proteins recruited at that interface. In contrast, much less is known about the fungal proteins involved in this process. Here, we have identified an AM fungal effector that participates in this developmental step of the symbiosis. RiCRN1 is a crinkler (CRN) effector that belongs to a subfamily of secreted CRN proteins from R. irregularis. CRNs have been so far only functionally characterized in pathogenic microbes and shown to participate in processes controlling plant cell death and immunity. RiCRN1 accumulates during symbiosis establishment parallel to MtPT4, the gene coding for an arbuscule-specific phosphate transporter. Expression in Nicotiana benthamiana leaves and in Medicago truncatula roots suggest that RiCRN1 is not involved in cell death processes. RiCRN1 dimerizes and localizes to nuclear bodies, suggesting that, similar to other CRNs, it functions in the plant nucleus. Downregulation of RiCRN1 using host-induced gene silencing led to an impairment of the symbiosis in M. truncatula and to a reduction of MtPT4, while ectopic expression of RiCRN1, surprisingly, led to a drastic reduction in arbuscule size that correlated with a decrease not only in MtPT4 but also in MtBCP1, a marker for initial stages of arbuscule development. Altogether, our results suggest that a tightly regulated expression in time and space of RiCRN1 is critical for symbiosis progression and for the proper initiation of arbuscule development.
Highlights
Most microbial activity in soils is concentrated in the rhizosphere, the area in close vicinity to the root and influenced by the secretion of plant substances
Sequencing of the R. irregularis genome (Tisserant et al, 2013; Lin et al, 2014) showed the existence of several entries with similarities to genes coding for CRN proteins, that had been first identified in oomycetes and chytridiomycota (Haas et al, 2009; Raffaele et al, 2010)
We show that Arbuscular Mycorrhiza mycorrhizal (AM) fungi contain a repertoire of putative CRN effectors that besides the SP7-like proteins represent a new family of effectors characterized in an AM fungus
Summary
Most microbial activity in soils is concentrated in the rhizosphere, the area in close vicinity to the root and influenced by the secretion of plant substances. A very recent study has even shown that the virulence activity of the Phytophthora capsici CRN83_152 in planta is not related to its cell death inducing activity (Amaro et al, 2018) All these results suggest that CRN proteins could have other functions besides cell death induction. While it has been shown that CRN translocation into plant cells is mediated by the LxLFLAK motif in the N-terminus (Schornack et al, 2010), the effector function of CRN proteins within the plant is ascribed to their C-terminal region (Liu et al, 2011; van Damme et al, 2012; Stam et al, 2013b). AeCRN13 is homolog to BdCRN13 from the animal pathogenic fungus B. dendrobatidis, and reciprocal expression in amphibians or plant cells induced aberrant cell development, suggesting a conserved mechanism of function for both effectors. Our data suggest a critical involvement of RiCRN1 proteins in the establishment of a functional symbiosis
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