scholarly journals Fungal jasmonate as a novel morphogenetic signal for pathogenesis

2021 ◽  
Author(s):  
Yingyao Liu ◽  
Martin Pagac ◽  
Fan Yang ◽  
Rajesh Narhari Patkar ◽  
Naweed I Naqvi

A key question that has remained unanswered is how pathogenic fungi switch from vegetative growth to infection-related morphogenesis during a disease cycle. Here, we identify a fungal oxylipin analogous to the well-known phytohormone jasmonic acid, as the principal morphogenesis signal responsible for such a developmental switch to pathogenicity in the rice-blast fungus Magnaporthe oryzae. We explored the molecular function(s) of such intrinsic jasmonic acid during pathogenic differentiation in M. oryzae via OPR1, which encodes a 12-Oxo-phytodienoic Acid Reductase essential for its biosynthesis. Loss of OPR1 led to prolonged vegetative growth, and a delayed initiation and improper development of infection structures in M. oryzae, reminiscent of phenotypes observed in mutants (e.g. pth11Δ and cpkAΔ) that are compromised for cyclic AMP signaling. Genetic- or chemical-complementation completely restored proper germ tube growth and appressorium formation in opr1Δ. Liquid chromatography mass spectrometry-based quantification revealed increased OPDA accumulation and a significant decrease in JA levels in the opr1Δ. Most interestingly, exogenous jasmonic acid also restored appressorium formation in the pth11Δ mutant that lacks G protein/cyclic AMP signaling. Epistasis analysis placed fungal jasmonate upstream of the cyclic AMP signaling in rice blast. Lastly, we show that intrinsic jasmonate orchestrates the cessation of vegetative phase and initiates pathogenic development via a regulatory interaction with the cyclic AMP cascade and redox signaling in rice blast.

2021 ◽  
Vol 7 (9) ◽  
pp. 693
Author(s):  
Yingyao Liu ◽  
Martin Pagac ◽  
Fan Yang ◽  
Rajesh N. Patkar ◽  
Naweed I. Naqvi

A key question that has remained unanswered is how pathogenic fungi switch from vegetative growth to infection-related morphogenesis during a disease cycle. Here, we identify a fungal oxylipin analogous to the phytohormone jasmonic acid (JA), as the principal regulator of such a developmental switch to isotropic growth and pathogenicity in the rice-blast fungus Magnaporthe oryzae. Using specific inhibitors and mutant analyses, we determined the molecular function of intrinsic jasmonates during M. oryzae pathogenesis. Loss of 12-Oxo-phytodienoic Acid (OPDA) Reductase and/or consequent reduction of jasmonate biosynthesis, prolonged germ tube growth and caused delayed initiation and improper development of infection structures in M. oryzae, reminiscent of phenotypic defects upon impaired cyclic AMP (cAMP) signaling. Chemical- or genetic-complementation completely restored proper vegetative growth and appressoria in opr1Δ. Mass spectrometry-based quantification revealed increased OPDA accumulation and significantly decreased jasmonate levels in opr1Δ. Most interestingly, exogenous jasmonate restored proper appressorium formation in pth11Δ that lacks G protein/cAMP signaling; but failed to do so in the Mitogen-activated protein (MAP) kinase mutants. Epistasis analysis placed jasmonate upstream of the cAMP pathway in rice blast. Mechanistically, intrinsic jasmonate orchestrates timely cessation of the vegetative phase and induces pathogenic development via a complex regulatory interaction with the cAMP-PKA cascade and redox signaling in rice blast.


2000 ◽  
Vol 90 (10) ◽  
pp. 1162-1168 ◽  
Author(s):  
Hong-Sik Oh ◽  
Yong-Hwan Lee

Chemical fungicides are a major method of control for plant diseases in spite of potential negative effects on the environment and the appearance of resistant strains. Development of new chemical fungicides has been largely dependent upon in vivo efficacy tests in the greenhouse or in fields, which is in contrast to target-oriented in vitro screening systems widely used in the pharmaceutical field. To establish a target-site—specific screening system for antifungal compounds, specific inhibition on appressorium formation of the rice blast fungus Magnaporthe grisea was employed. For many plant-pathogenic fungi, including M. grisea, appressorium formation is an essential step to infect host plants. Among 1,000 culture filtrates of members of the class Actinomycetes and fungi, five (A5005, A5008, A5314, A5387, and A5397) from the class Actinomycetes showed differential inhibitory effects on appressorium formation of M. grisea in a dosage-dependent manner. Three (A5005, A5314, and A5387) of these were further fractionated into ethyl acetate and water fractions. The ethyl acetate fraction of A5005 and both the ethyl acetate and water fractions from A5314 and A5387 inhibited appressorium formation, while conidial germination remained little affected. Inhibition of appressorium formation by the ethyl acetate or water fraction was reversed by the exogenous addition of cyclic AMP. Significantly reduced numbers of conidia with appressoria were observed on rice leaves in the presence of culture filtrates. Furthermore, these culture filtrates also exhibited significant disease control of rice blast in the greenhouse. This rapid and target-oriented screening system could be adopted to screen candidate compounds for rice blast control and could be applicable for other appressorium-forming, plant-pathogenic fungi.


2019 ◽  
Vol 47 (6) ◽  
pp. 1733-1747 ◽  
Author(s):  
Christina Klausen ◽  
Fabian Kaiser ◽  
Birthe Stüven ◽  
Jan N. Hansen ◽  
Dagmar Wachten

The second messenger 3′,5′-cyclic nucleoside adenosine monophosphate (cAMP) plays a key role in signal transduction across prokaryotes and eukaryotes. Cyclic AMP signaling is compartmentalized into microdomains to fulfil specific functions. To define the function of cAMP within these microdomains, signaling needs to be analyzed with spatio-temporal precision. To this end, optogenetic approaches and genetically encoded fluorescent biosensors are particularly well suited. Synthesis and hydrolysis of cAMP can be directly manipulated by photoactivated adenylyl cyclases (PACs) and light-regulated phosphodiesterases (PDEs), respectively. In addition, many biosensors have been designed to spatially and temporarily resolve cAMP dynamics in the cell. This review provides an overview about optogenetic tools and biosensors to shed light on the subcellular organization of cAMP signaling.


2020 ◽  
Vol 21 (22) ◽  
pp. 8681
Author(s):  
Nicolò Orsoni ◽  
Francesca Degola ◽  
Luca Nerva ◽  
Franco Bisceglie ◽  
Giorgio Spadola ◽  
...  

As key players in biotic stress response of plants, jasmonic acid (JA) and its derivatives cover a specific and prominent role in pathogens-mediated signaling and hence are promising candidates for a sustainable management of phytopathogenic fungi. Recently, JA directed antimicrobial effects on plant pathogens has been suggested, supporting the theory of oxylipins as double gamers in plant-pathogen interaction. Based on these premises, six derivatives (dihydrojasmone and cis-jasmone, two thiosemicarbazonic derivatives and their corresponding complexes with copper) have been evaluated against 13 fungal species affecting various economically important herbaceous and woody crops, such as cereals, grapes and horticultural crops: Phaeoacremonium minimum, Neofusicoccum parvum, Phaeomoniella chlamydospora, Fomitiporia mediterranea, Fusarium poae, F. culmorum, F. graminearum, F. oxysporum f. sp. lactucae,F. sporotrichioides, Aspergillus flavus, Rhizoctonia solani,Sclerotinia spp. and Verticillium dahliae. The biological activity of these compounds was assessed in terms of growth inhibition and, for the two mycotoxigenic species A. flavus and F. sporotrichioides, also in terms of toxin containment. As expected, the inhibitory effect of molecules greatly varied amongst both genera and species; cis-jasmone thiosemicarbazone in particular has shown the wider range of effectiveness. However, our results show that thiosemicarbazones derivatives are more effective than the parent ketones in limiting fungal growth and mycotoxins production, supporting possible applications for the control of pathogenic fungi.


2002 ◽  
Vol 22 (12) ◽  
pp. 3981-3993 ◽  
Author(s):  
Xuewen Pan ◽  
Joseph Heitman

ABSTRACT The yeast Saccharomyces cerevisiae undergoes a dimorphic filamentous transition in response to nutrient cues that is affected by both mitogen-activated protein kinase and cyclic AMP-protein kinase A signaling cascades. Here two transcriptional regulators, Flo8 and Sfl1, are shown to be the direct molecular targets of protein kinase A. Flo8 and Sfl1 antagonistically control expression of the cell adhesin Flo11 via a common promoter element. Phosphorylation by the protein kinase A catalytic subunit Tpk2 promotes Flo8 binding and activation of the Flo11 promoter and relieves repression by prohibiting dimerization and DNA binding by Sfl1. Our studies illustrate in molecular detail how protein kinase A combinatorially effects a key developmental switch. Similar mechanisms may operate in pathogenic fungi and more complex multicellular eukaryotic organisms.


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