A feed-forward subnetwork emerging from integrated TOR-and cAMP/PKA-signaling architecture reinforces magnaporthe oryzae appressorium morphogenesis

Guangchao Sun, Xiaobo Qi, Richard A. Wilson

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Appressoria are important mediators of plant-microbe interactions. In the devastating rice blast pathogen Magnaporthe oryzae, appressorial morphogenesis from germ tube tips requires activated cAMP/PKA signaling and inactivated TOR signaling (TORoff). TORoff temporarily arrests G2 at a metabolic checkpoint during the single round of mitosis that occurs following germination. G2 arrest induces autophagy and appressorium formation concomitantly, allowing reprogression of the cell cycle to G1/G0 quiescence and a single appressorial nucleus. Inappropriate TOR activation abrogates G2 arrest and inhibits cAMP/PKA signaling downstream of cPKA. This results in multiple rounds of germ tube mitosis and the loss of autophagy and appressoria formation. How cAMP/PKA signaling connects to cell cycle progression and autophagy is not known. To address this, we interrogated TOR and cAMP/PKA pathways using signaling mutants, different surface properties, and specific cell cycle inhibitors and discovered a feed-forward subnetwork arising from TOR-and cAMP/PKA-signaling integration. This adenylate cyclase-cAMP-TOR-adenylate cyclase subnetwork reinforces cAMP/PKA-dependent appressorium formation under favorable environmental conditions. Under unfavorable conditions, the subnetwork collapses, resulting in reversible cell cycle-mediated germ tube growth regardless of external nutrient status. Collectively, this work provides new molecular insights on germ tube morphogenetic decision-making in response to static and dynamic environmental conditions.

Original languageEnglish (US)
Pages (from-to)593-607
Number of pages15
JournalMolecular Plant-Microbe Interactions
Volume32
Issue number5
DOIs
StatePublished - May 2019

ASJC Scopus subject areas

  • Physiology
  • Agronomy and Crop Science

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