Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants

Abstract

Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungusRhizophagus irregularisremarkably promoted rice (Oryza sativa) growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO3−supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter geneOsNPF4.5in rice roots, and its orthologsZmNPF4.5inZea maysandSbNPF4.5inSorghum bicolor. OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO3−transport activity when expressed inXenopus laevisoocytes. Moreover, knockout ofOsNPF4.5resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO3−was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO3−acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species.

Genome-Wide Systematic Characterization of the NPF Family Genes and Their Transcriptional Responses to Multiple Nutrient Stresses in Allotetraploid Rapeseed

“…Nitrate uptake is carried out by plasma membrane-located nitrate transporters, such as OsNPF4;5 [ 28 ]. In B. napus , we performed the subcellular localization analyses of BnaNPF proteins using the WoLF PSORT program.…”

“…Interestingly, OsNRT1.1B , the functional homologue of AtNRT1.1 in rice, can function not only in mediating nitrate signal transduction from the plasma membrane to the nucleus, but also in integrating the nitrate and phosphate signaling networks, as well as in regulating the root microbiota to facilitate organic N mineralization in soil [ 26 , 27 ]. Very recently, Wang et al (2020) found that OsNPF4.5 plays a key role in mycorrhizal NO 3 − acquisition [ 28 ]. These studies suggest that NPFs play important roles in plant developmental processes.…”

Identification of a unique ZIP transporter involved in zinc uptake via the arbuscular mycorrhizal fungal pathway

“…through exudation that mobilises Zn in soil) that led to increased plant uptake of Zn via the direct pathway. (21). This suggests that the plant-fungal symbiosis is somewhat disrupted by the loss of MtZIP14 expression, and that the active sites of nutrient transport (arbuscules), as well as fungal resource storage units (vesicles), were not able to be produced by the fungus to the same extent due to this disruption.…”

“…Considerable progress has been made toward identifying the components involved in P and N AM associations (19)(20)(21), and a AM-specific plant Cu transporter has been recently identified (22). In order to fully exploit the AM symbiosis for improved agricultural outcomes (i.e.…”

Cross-ecosystem transcriptomics identifies distinct genetic modules for nutrient acquisition in maize

“…Deficiencies in P and N trigger secretion of the plant hormone strigolactones into the rhizosphere (22), which facilitates contact of fungal hyphae with the roots via stimulating hyphal branching (23). After the physical contact, the fungal hyphae grow into the cortex and form the highly-branched hyphal termini "arbuscules" where nutrient exchange between the symbionts occurs; briefly, Pi, nitrate, and ammonium are taken up from the soil by extraradical hyphae, delivered to the arbuscules, and released into the arbuscular interface (reviewed in 24) from which the plant cell takes up the nutrients via the mycorrhiza-specific transporters for Pi (25,26), nitrate (27), and ammonium (28). In return, the host supplies lipid (29)(30)(31)(32) and sugar (33) as carbon source for the fungi via the complex of half-size ABC transporters STR/STR2, a putative lipid exporter (34), and the sugar transporter SWEET (35), respectively.…”