Nonredundant Regulation of Rice Arbuscular Mycorrhizal Symbiosis by Two Members of the PHOSPHATE TRANSPORTER1 Gene Family

Abstract

Pi acquisition of crops via arbuscular mycorrhizal (AM) symbiosis is becoming increasingly important due to limited highgrade rock Pi reserves and a demand for environmentally sustainable agriculture. Here, we show that 70% of the overall Pi acquired by rice (Oryza sativa) is delivered via the symbiotic route. To better understand this pathway, we combined genetic, molecular, and physiological approaches to determine the specific functions of two symbiosis-specific members of the PHOSPHATE TRANSPORTER1 (PHT1) gene family from rice, ORYsa;PHT1;11 (PT11) and ORYsa;PHT1;13 (PT13). The PT11 lineage of proteins from mono-and dicotyledons is most closely related to homologs from the ancient moss, indicating an early evolutionary origin. By contrast, PT13 arose in the Poaceae, suggesting that grasses acquired a particular strategy for the acquisition of symbiotic Pi. Surprisingly, mutations in either PT11 or PT13 affected the development of the symbiosis, demonstrating that both genes are important for AM symbiosis. For symbiotic Pi uptake, however, only PT11 is necessary and sufficient. Consequently, our results demonstrate that mycorrhizal rice depends on the AM symbiosis to satisfy its Pi demands, which is mediated by a single functional Pi transporter, PT11.

Phosphate Treatment Strongly Inhibits New Arbuscule Development But Not the Maintenance of Arbuscule in Mycorrhizal Rice Roots

“…Specifically, P selectively inhibited the development of new arbuscules without compromising the life cycle of finely branched arbuscules or eliminating the intraradical accommodation of AM fungi. Importantly, the reduction of arbuscule density with P was accelerated in the rice pt11-1 mutant, which is defective in P uptake after release from arbuscule branches (Yang et al, 2012). These observations suggest a novel regulatory mode of intraradical colonization that is mycelium-type specific during P inhibition.…”

“…To further confirm the stability of branched arbuscules during P inhibition, arbuscule sizes were analyzed using the GFP-fused rice phosphate transporter PT11, which is specifically located on periarbuscular membranes surrounding arbuscule branches (Kobae and Hata, 2010; and is responsible for phosphate uptake in the rice mycorrhizal pathway (Yang et al, 2012). The size of arbuscules indicated by PT11-GFP was not affected by P treatment at 5 h after the treatment (Fig.…”

“…Calculations of the contribution of P uptake via AM fungi (mycorrhizal pathway) to total plant P uptake suggest that mycorrhizal pathways dominate total P uptake under low P conditions (Smith et al, 2004;Yang et al, 2012). Accordingly, mycorrhizal symbiosis downregulates plant P transporter genes that may contribute to the direct pathway involving P uptake at the root epidermis or root hairs (Javot et al, 2007;Walder et al, 2015).…”

Phylogenetic, structural, and functional characterization of AMT3;1, an ammonium transporter induced by mycorrhization among model grasses

“…In M. truncatula mutants lacking MtPT4, a phosphate transporter (PHT) located in the periarbuscular membrane and essential for symbiotic Pi transport (Harrison et al 2002), arbuscules are prematurely degenerated and the symbiosis is not maintained (Javot et al 2007). Similarly, in rice plants lacking PT11, the PHT responsible for symbiotic phosphate (Pi) transfer in rice showed a strongly reduced colonization and arbuscule level (Yang et al 2012). The Poaceae split into two major clades: the BEP and PACCMAD clades (Bouchenak-Khelladi et al 2008;Glémin and Bataillon 2009) (Fig.…”

Genetic approaches to enhancing phosphorus-use efficiency (PUE) in crops: challenges and directions

“…The functional roles of the two new mycorrhizal-specific barley Pi transporters in P acquisition remain to be revealed. Two mycorrhizal-specific Pi transporters have been identified in rice (Yang et al 2012) and one in barrel medic (Medicago truncatula Gaertn.) (Javot et al 2007).…”