Aquaporin‐mediated long‐distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus‐induced gene silencing

Abstract

SummaryArbuscular mycorrhizal fungi translocate polyphosphate through hyphae over a long distance to deliver to the host. More than three decades ago, suppression of host transpiration was found to decelerate phosphate delivery of the fungal symbiont, leading us to hypothesize that transpiration provides a primary driving force for polyphosphate translocation, probably via creating hyphal water flow in which fungal aquaporin(s) may be involved.The impact of transpiration suppression on polyphosphate translocation through hyphae of Rhizophagus clarus was evaluated. An aquaporin gene expressed in intraradical mycelia was characterized and knocked down by virus-induced gene silencing to investigate the involvement of the gene in polyphosphate translocation.Rhizophagus clarus aquaporin 3 (RcAQP3) that was most highly expressed in intraradical mycelia encodes an aquaglyceroporin responsible for water transport across the plasma membrane. Knockdown of RcAQP3 as well as the suppression of host transpiration decelerated polyphosphate translocation in proportion to the levels of knockdown and suppression, respectively.These results provide the first insight into the mechanism underlying long-distance polyphosphate translocation in mycorrhizal associations at the molecular level, in which host transpiration and the fungal aquaporin play key roles. A hypothetical model of the translocation is proposed for further elucidation of the mechanism.

Connecting polyphosphate translocation and hyphal water transport points to a key of mycorrhizal functioning

“…Cooper & Tinker () had proposed that transpiration impacts photosynthesis via substrate limitation through stomata and, in consequence, the carbohydrate supply of the fungus, which limits energy‐dependent polyphosphate translocation towards the plant. In the current paper, Kikuchi et al . raised two new hypotheses. First, they postulated that polyphosphate translocation does not depend on the energy status of the fungus.…”

“…Among all mineral nutrients, phosphate plays a major role in the AM symbiosis. Tatsuhiro Ezawa, the corresponding author of the current paper Kikuchi et al ., in this issue of New Phytologist (pp. 1202–1208), has worked since the 1990s on phosphate metabolism and transport in AM fungal hyphae.…”

Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria

“…The improved P nutrition of mycorrhizal plants is also the result of hyphal P uptake beyond the P depletion zone caused by the fast root absorption of P from the soil solution, which cannot be rapidly replenished, given the poor mobility of P in the soil 8, 10 . The P taken up by ERM is translocated to intraradical hyphae in the form of polyphosphates 24–26 . High P fluxes in AMF hyphae have been detected, ranging from 2 to 20 × 10 −6  mol m −2 s −1  27–29 , with bidirectional protoplasmic flows, measured on the basis of cellular particles movement (vacuoles, nuclei, fat droplets, organelles, granules), ranging from 3.0 to 4.3 μm s −1  30, 31 .…”

Arbuscular mycorrhizal symbiosis-mediated tomato tolerance to drought

“…Furthermore, a role of host transpiration and fungal AQP in long-distance fungal polyphosphate (polyP) translocation, and consequently on fungal phosphate (Pi) delivery, has been recently proposed. 21 The data obtained in our recent publication, 8 showing a change in plant performance in the presence of the AM fungi under WS, offer new insights for understanding the molecular and physiological mechanisms underlying the tomato tolerance to drought as mediated by the AM fungi. Together with experiments performed by several researchers in the last years, they also open new perspectives in the exploitation of AM symbiosis to enhance crop tolerance to abiotic stress in a scenario of climate change.…”