The TOR signalling pathway in fungal phytopathogens: A target for plant disease control

Abstract

Plant diseases caused by fungal phytopathogens have led to significant economic losses in agriculture worldwide. The management of fungal diseases is mainly dependent on the application of fungicides, which are not suitable for sustainable agriculture, human health, and environmental safety. Thus, it is necessary to develop novel targets and green strategies to mitigate the losses caused by these pathogens. The target of rapamycin (TOR) complexes and key components of the TOR signalling pathway are evolutionally conserved in pathogens and closely related to the vegetative growth and pathogenicity. As indicated in recent systems, chemical, genetic, and genomic studies on the TOR signalling pathway, phytopathogens with TOR dysfunctions show severe growth defects and nonpathogenicity, which makes the TOR signalling pathway to be developed into an ideal candidate target for controlling plant disease. In this review, we comprehensively discuss the current knowledge on components of the TOR signalling pathway in microorganisms and the diverse roles of various plant TOR in response to plant pathogens. Furthermore, we analyse a range of disease management strategies that rely on the TOR signalling pathway, including genetic modification technologies and chemical controls. In the future, disease control strategies based on the TOR signalling network are expected to become a highly effective weapon for crop protection.

Keywords: TOR signalling pathway; disease control; plant pathogens.

FIGURE 1

Structures and complexes of TOR kinase in the model fungi Saccharomyces cerevisiae and Schizosaccharomyces pombe. (a) Conserved domain structure of TOR kinase. TOR kinase domain architecture is highly conserved. TOR contains the N‐terminal clusters of huntingtins, elongation factor 3, a subunit of protein phosphatase 2A and TOR1 (HEAT) repeats, followed by a FRAP, ATM, and TRRAP (FAT) domain; the FKBP12–rapamycin binding (FRB) domain; the catalytic kinase domain; and the C‐terminal FATC domain. (b) Components of TORC1 and TORC2 in S. cerevisiae, S. pombe, and two well‐studied representative plant‐pathogenic fungi Fusarium graminearum and Magnaporthe oryzae. Rapamycin (RAP)‐FKBP12 complex binds to the TORC1 complex, instead of the TORC2 complex. AVO1/2/3, adheres stroly (to TOR2) 1/2/3; BIT61, binding partner of TOR2 protein 61; KOG1, kontroller of growth 1; LST8, lethal with SEC. 13 protein 8; SIN1, MAPK‐interacting protein 1; STE20, a homologue of AVO1; TCO89, TOR complex one 89; TOR, target of rapamycin; TORC1, TOR complex 1; TORC2, TOR complex 2; WAT1, a homologue of LST8.

FIGURE 2

TOR signalling pathway governs key processes that strikingly affect fungal pathogenesis. Components of the TOR pathway in Botrytis cinerea (a), Fusarium graminearum (b), Fusarium oxysporum (c), Magnaporthe oryzae (d), Phytophthora infestans (e), Verticillium dahliae (f), and other representative plant‐pathogenic fungi (g) are shown. ABL1, carbon‐responsive gene; AreA, global nitrogen regulator; ASD4, the GATA transcription factor‐encoding gene; CAK1, protein kinase; cAMP, monobutyryl cyclic AMP; CaMV, cauliflower mosaic virus; FKBP12, FK506 binding protein 12; GAP1, amino acid permease; IMP1, vacuolar protein required for membrane trafficking; LST8, lethal with SEC. 13 protein 8; MAC1, the adenylate cyclase; MeaB, bZIP protein; MGV1, mitogen‐activated protein kinase gene 1; MKK1, mitogen‐activated protein kinase (MAPK) kinase; MSG5, phosphatase similar to yeast Msg5; NEM, protein phosphatase; NUT1, a major nitrogen regulatory gene; PAH, phosphatidate phosphatase; PKA, protein kinase A; PMP1, a tyrosine‐protein phosphatase; PP2A, protein phosphatase 2A; PPE1, homologue to Saccharomyces cerevisiae Sit4/Ppe1; PR1, pathogenesis‐related protein 1; R. solanacearum, Ralstonia solanacearum; RAP, rapamycin; RAPTOR, regulatory‐associated protein of mTOR; ROS, reactive oxygen species; RRD, resistance to rapamycin deletion 2; SIT4, PP2A phosphatase; SNF1, sucrose non‐fermenting 1; SNT2, named for the presence of the DNA‐binding domain SaNT; STRIPAK, striatin‐interacting phosphatases and kinases; TAP42, Tor associated protein 42; TIP41, Tap42‐interacting protein 41; TOR, target of rapamycin; VAST, VASt domain‐containing protein; WHI2, a homologue of S. cerevisiae Whi2 (Whisky2); X. citri, Xanthomonas citri.

FIGURE 3

Pathogens affect the plant TOR signalling to drive their infection. Pathogens can recruit plant TOR/S6K1 signalling to facilitate their growth. TOR inhibition through inhibitor treatments, RNAi, or VIGS technologies primes immunity and pathogen resistance in plants. CaMV, cauliflower mosaic virus; Pst, Pseudomonas syringae pv. tomato; R. solanacearum, Ralstonia solanacearum; X. citri, Xanthomonas citri; TOR, target of rapamycin; S6K1, ribosomal protein S6 kinase; TAV, transactivator–viroplasmin; RNAi, RNA interference; RISP, reinitiation‐supporting protein; AWR5, type III effector; SA, salicylic acid; P6, a versatile viral effector; PthA4, a transcription activator‐like (TAL) effector; AvrRpm1, a Pseudomonas effector; VIGS, virus‐induced gene silencing.

FIGURE 4

Schematic illustration of TOR‐based therapies for disease control. Genetic modification technology and biopesticide mentioned here are based on the literature survey conducted on the papers published recently. Whether and how some new technologies such as engineered nanoparticles or functional peptides can be applied to TOR‐based therapies needs further investigation.