Abstract
Fungal plant pathogens are persistent and global food security threats. To invade their hosts they often form highly specialized infection structures, known as appressoria. The cAMP/ PKA- and MAP kinase-signaling cascades have been functionally delineated as positive-acting pathways required for appressorium development. Negative-acting regulatory pathways that block appressorial development are not known. Here, we present the first detailed evidence that the conserved Target of Rapamycin (TOR) signaling pathway is a powerful inhibitor of appressorium formation by the rice blast fungus Magnaporthe oryzae. We determined TOR signaling was activated in an M. oryzae mutant strain lacking a functional copy of the GATA transcription factor-encoding gene ASD4. Δasd4 mutant strains could not form appressoria and expressed GLN1, a glutamine synthetase-encoding orthologue silenced in wild type. Inappropriate expression of GLN1 increased the intracellular steady-state levels of glutamine in Δasd4 mutant strains during axenic growth when compared to wild type. Deleting GLN1 lowered glutamine levels and promoted appressorium formation by Δasd4 strains. Furthermore, glutamine is an agonist of TOR. Treating Δasd4 mutant strains with the specific TOR kinase inhibitor rapamycin restored appressorium development. Rapamycin was also shown to induce appressorium formation by wild type and Δcpka mutant strains on non-inductive hydrophilic surfaces but had no effect on the MAP kinase mutant Δpmk1. When taken together, we implicate Asd4 in regulating intracellular glutamine levels in order to modulate TOR inhibition of appressorium formation downstream of cPKA. This study thus provides novel insight into the metabolic mechanisms that underpin the highly regulated process of appressorium development.
Highlights
Fungal pathogens cause some of the most devastating crop diseases and constitute globe-wide challenges to socioeconomic growth and food security
We provide evidence that a mutant M. oryzae strain, unable to form appressoria, accumulates intracellular glutamine that, in turn, inappropriately activates a conserved signaling pathway called target of rapamycin (TOR)
In a previous study [18], we showed that the GATA family [19] transcription factor Asd4 was essential for sporulation, optimal growth on undefined complete media (CM) and appressorium formation [18]
Summary
Fungal pathogens cause some of the most devastating crop diseases and constitute globe-wide challenges to socioeconomic growth and food security. To facilitate entry into their hosts, many filamentous pathogens form highly specialized infection structures, known as appressoria, on the leaf surface [1 – 3]. Appressoria breach the host cuticle and allow access to the underlying epidermal cells. In addition to facilitating plant invasion, appressoria can act as sites of effector delivery and mediate the molecular host-pathogen interaction [6, 7]. Despite their widespread occurrence and long-acknowledged importance to plant health, detailed mechanistic descriptions of the regulatory pathways necessary for appressorium formation are limited to two molecular pathways, the cAMP/ PKA- and MAP kinase—signaling cascades [2, 5, 8 – 10]
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