Host-related metabolic cues affect colonization strategies of a root endophyte

Abstract

The mechanisms underpinning broad compatibility in root symbiosis are largely unexplored. The generalist root endophyte Piriformospora indica establishes long-lasting interactions with morphologically and biochemically different hosts, stimulating their growth, alleviating salt stress, and inducing local and systemic resistance to pathogens. Cytological studies and global investigations of fungal transcriptional responses to colonization of barley and Arabidopsis at different symbiotic stages identified host-dependent colonization strategies and host-specifically induced effector candidates. Here, we show that in Arabidopsis, P. indica establishes and maintains biotrophic nutrition within living epidermal cells, whereas in barley the symbiont undergoes a nutritional switch to saprotrophy that is associated with the production of secondary thinner hyphae in dead cortex cells. Consistent with a diversified trophic behavior and with the occurrence of nitrogen deficiency at the onset of saprotrophy in barley, fungal genes encoding hydrolytic enzymes and nutrient transporters were highly induced in this host but not in Arabidopsis. Silencing of the high-affinity ammonium transporter PiAMT1 gene, whose transcripts are accumulating during nitrogen starvation and in barley, resulted in enhanced colonization of this host, whereas it had no effect on the colonization of Arabidopsis. Increased levels of free amino acids and reduced enzymatic activity for the cell-death marker VPE (vacuolar-processing enzyme) in colonized barley roots coincided with an extended biotrophic lifestyle of P. indica upon silencing of PiAMT1. This suggests that PiAmt1 functions as a nitrogen sensor mediating the signal that triggers the in planta activation of the saprotrophic program. Thus, host-related metabolic cues affect the expression of P. indica's alternative lifestyles.root cortical cell death | RCD | broad-host range | biotrophy | mutualism U pon plant colonization, fungi adopt different strategies to gain access to host nutrients. Whereas necrotrophs kill plant cells with subsequent saprotrophic nutrition, other fungi maintain biotrophic relationships with their hosts either transiently (hemibiotrophs) or as lifelong interactions. The degree of specialization to a particular host and the host's metabolic status may greatly influence plant colonization (1-4). Broad-host range root endophytes undergo long-term interactions with a large variety of plants, thereby playing a significant role in natural and managed ecosystems and in the evolution of land plants. To establish and maintain a compatible interaction with different hosts, these endophytes must respond and adapt to host-specific signals. Alternative lifestyles and colonization strategies in different host species thus may be a consequence of this adaptation to highly variable host environments. In this study, we addressed the question of whether endophytes adopt different strategies during colonization of distinct hosts or whether their success resides in a general colonization st...

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

“…Two to three weeks after inoculation, plants showed a significant increase in shoot and root fresh weight (FW), and strongly accelerated lateral root formation, regardless of the substrate in which they were grown (Supplementary Figures S2a-f). This finding adds another level of complexity to the yet controversial discussion as to whether P. indica induces biomass formation in Brassicaceae (Lahrmann et al, 2013). Our data doubtless show that the bacterial partner of P. indica is able to strongly induce growth promotion in Arabidopsis.…”

The fungal-specific β-glucan-binding lectin FGB1 alters cell-wall composition and suppresses glucan-triggered immunity in plants

“…In order to identify possible compatibility factors in the interaction of P. indica with different hosts, we recently performed global characterization of fungal transcriptional responses to barley and Arabidopsis at different developmental stages1112. The majority of induced genes encoding small secreted proteins (SSPs; <300 amino acids), which are possibly enriched in effectors13, were either barley or Arabidopsis responsive, suggesting that colonization of different hosts might require exploitation of host dependently induced effectors that interact with elements characteristic to each host1114.…”

“…The initial biotrophic phase is followed by a stage where the fungus is more often found in dead or dying host cells secreting a large variety of hydrolytic enzymes that degrade plant cell walls and proteins. This is especially evident in barley where the symbiont rapidly undergoes a nutritional switch to saprotrophy that correlates with nitrogen limitation and is associated with the production of thinner hyphae in dead root cells11.…”

Effect of root colonization with Piriformospora indica and phosphate availability on the growth and reproductive biology of a Cyclamen persicum cultivar

“…(Franken, 2012(Franken, , p. 1458. Thus, the colonization strategies and trophic behavior of P. indica were affected by host-related metabolic cues and nutrient availability (Lahrmann et al, 2013). In Cyclamen, these host-plant and environment-specific P. indica actions may have resulted in P contents in plants that remained unaffected even under a deficient P availability, as well as boosted P contents under an ample P supply.…”