Expression Pattern Suggests a Role of MiR399 in the Regulation of the Cellular Response to Local Pi Increase During Arbuscular Mycorrhizal Symbiosis

Abstract

Many plants improve their phosphate (Pi) availability by forming mutualistic associations with arbuscular mycorrhizal (AM) fungi. Pi-repleted plants are much less colonized by AM fungi than Pi-depleted plants. This indicates a link between plant Pi signaling and AM development. MicroRNAs (miR) of the 399 family are systemic Pi-starvation signals important for maintenance of Pi homeostasis in Arabidopsis thaliana and might also qualify as signals regulating AM development in response to Pi availability. MiR399 could either represent the systemic low-Pi signal promoting or required for AM formation or they could act as counter players of systemic Pi-availability signals that suppress AM symbiosis. To test either of these assumptions, we analyzed the miR399 family in the AM-capable plant model Medicago truncatula and could experimentally confirm 10 novel MIR399 genes in this species. Pi-depleted plants showed increased expression of mature miR399 and multiple pri-miR399, and unexpectedly, levels of five of the 15 pri-miR399 species were higher in leaves of mycorrhizal plants than in leaves of nonmycorrhizal plants. Compared with nonmycorrhizal Pi-depleted roots, mycorrhizal roots of Pi-depleted M. truncatula and tobacco plants had increased Pi contents due to symbiotic Pi uptake but displayed higher mature miR399 levels. Expression levels of MtPho2 remained low and PHO2-dependent Pi-stress marker transcript levels remained high in these mycorrhizal roots. Hence, an AM symbiosis-related signal appears to increase miR399 expression and decrease PHO2 activity. MiR399 overexpression in tobacco suggested that miR399 alone is not sufficient to improve mycorrhizal colonization supporting the assumption that, in mycorrhizal roots, increased miR399 are necessary to keep the MtPho2 expression and activity low, which would otherwise increase in response to symbiotic Pi uptake.

Transgenic Plants That Express the Phytoplasma Effector SAP11 Show Altered Phosphate Starvation and Defense Responses

“…In the case of phytoplasmas, although the correlation between Pi and the disease symptoms remains unclear, the disease symptoms in phytoplasma-infected plants could be reduced by the application of AM fungi (Lingua et al, 2002;Romanazzi et al, 2009;Kami nska et al, 2010;Sampò et al, 2012). AM fungi are symbiotic organisms that are able to enhance the uptake of Pi through up-regulation of Pi starvation responses in host plants (Branscheid et al, 2010;Gu et al, 2010;Volpe et al, 2013). Thus, it will be interesting to explore whether the application of Pi could reduce the phytoplasma-mediated disease symptoms in the future.…”

Small Non-Coding RNAs in Plant Immunity

“…However these m i R N A s w e r e a l s o r e g u l a t e d b y p h o s p h a t e , p o i n t i n g t o a d i r e c t c o n n e c t i o n b e t w e e n nutrition and symbiosis. Previous studies demonstrated an induction of miR399 under Pi depleted conditions in mycorrhizal M. truncatula and tobacco plants associated with a concomitant increase in Pi content [102] …”

In silico identification and characterization of conserved plant microRNAs in barley

“…It is up-regulated upon Pi starvation to increase the uptake of Pi in Arabidopsis. Overexpression of miR399 causes Pi accumulation in shoots that display Pi toxicity symptoms [39][40][41]. miR396 regulates cell proliferation in developing leaves through the repression of GRF activity and a decrease in the expression of cell cycle genes [42].…”