Mechanisms and Impact of Symbiotic Phosphate Acquisition

Abstract

Phosphorous is important for life but often limiting for plants. The symbiotic pathway of phosphate uptake via arbuscular mycorrhizal fungi (AMF) is evolutionarily ancient and today occurs in natural and agricultural ecosystems alike. Plants capable of this symbiosis can obtain up to all of the phosphate from symbiotic fungi, and this offers potential means to develop crops less dependent on unsustainable P fertilizers. Here, we review the mechanisms and insights gleaned from the fine-tuned signal exchanges that orchestrate the intimate mutualistic symbiosis between plants and AMF. As the currency of trade, nutrients have signaling functions beyond being the nutritional goal of mutualism. We propose that such signaling roles and metabolic reprogramming may represent commitments for a mutualistic symbiosis that act across the stages of symbiosis development.

Inoculation with the mycorrhizal fungus Rhizophagus irregularis modulates the relationship between root growth and nutrient content in maize (Zea mays ssp. mays L.)

“…The growth increase in inoculated plants was likely driven by increased P uptake, given that the experiment was conducted under low P availability. The route of P from soil to fungus, and subsequent delivery to the plant host is well characterized (Chiu and Paszkowski, 2019). We saw clear evidence that a unit of mycorrhizal root translates to a greater quantity of P obtained than an equivalent unit of non-colonized root, as would be anticipated as a consequence of hyphal foraging (Fig.…”

“…AM fungi are obligate symbionts, obtaining carbon from their plant host in return for providing nutrients and water that are acquired by an extensive network of root-external hyphae (Bago et al, 2003). The clearest benefit to the plant is enhanced P uptake (Chiu and Paszkowski, 2019), although AM fungi have been reported to promote uptake of other elements, including N, Fe, S and Zn (Liu et al, 2000; González-Guerrero et al, 2005; Govindarajulu et al, 2005; López-Pedrosa and González-Guerrero, 2006; Allen and Shachar-Hill, 2009). In practice, complex interactions between nutrients influence the outcome of the symbiosis with respect to any given element (Liu et al, 2000; Gerlach et al, 2015; Ramírez-Flores et al, 2017).…”

“…Such a comparison, however, does not distinguish direct hyphal nutrient delivery from the secondary consequences of fungus-induced modification of root architecture or the effects of greater root growth resulting from a general increase in plant vigor. In the case of P, elegant labelling experiments and extensive functional studies have clearly demonstrated the direct role of root-external hyphae in nutrient delivery (Pearson and Jakobsen, 1993; Smith et al, 2003; Chiu and Paszkowski, 2019). The picture, however, remains less clear with respect to other mineral nutrients.…”

Identity and functions of inorganic and inositol polyphosphates in plants

“…PolyPs control the cell cycle by providing the Pi required for nucleotide synthesis during DNA replication (Bru et al, 2016). Outside the vacuole, polyPs have been observed in the fungal cell wall, where they are thought to play a role in providing Pi in symbiotic interactions (Chiu & Paszkowski, 2019) and protecting fungal cells from pathogens and toxic compounds (Werner et al, 2007b).…”

Inoculation with the mycorrhizal fungus Rhizophagus irregularis modulates the relationship between root growth and nutrient content in maize (Zea mays ssp. mays L.)

“…AM fungi are obligate symbionts, obtaining carbon from their plant host in return for providing nutrients and water that are acquired by an extensive network of root‐external hyphae (Bago et al, ). The clearest benefit to the plant is enhanced P uptake (Chiu & Paszkowski, ), although AM fungi have been reported to promote uptake of other elements, including N, Fe, S, and Zn (Allen & Shachar‐Hill, ; González‐Guerrero et al, ; Govindarajulu et al, ; Liu, Hamel, Hamilton, Ma, & Smith, ; López‐Pedrosa & González‐Guerrero, ). In practice, complex interactions between nutrients influence the outcome of the symbiosis with respect to any given element (Gerlach et al, ; Liu et al, ; Ramírez‐Flores et al, ).…”