Alternaria host-specific (HSTs) toxins: An overview of chemical characterization, target sites, regulation and their toxic effects

Abstract

Alternaria causes pathogenic disease on various economically important crops having saprophytic to endophytic lifecycle. Pathogenic fungi of Alternaria species produce many primary and secondary metabolites (SMs). Alternaria species produce more than 70 mycotoxins. Several species of Alternaria produce various phytotoxins that are host-specific (HSTs) and non-host-specific (nHSTs). These toxins have various negative impacts on cell organelles including chloroplast, mitochondria, plasma membrane, nucleus, Golgi bodies, etc. Non-host-specific toxins such as tentoxin (TEN), Alternaric acid, alternariol (AOH), alternariol 9-monomethyl ether (AME), brefeldin A (dehydro-), Alternuene (ALT), Altertoxin-I, Altertoxin-II, Altertoxin-III, zinniol, tenuazonic acid (TeA), curvularin and alterotoxin (ATX) I, II, III are known toxins produced by Alternaria species. In other hand, Alternaria species produce numerous HSTs such as AK-, AF-, ACT-, AM-, AAL- and ACR-toxin, maculosin, destruxin A, B, etc. are host-specific and classified into different family groups. These mycotoxins are low molecular weight secondary metabolites with various chemical structures. All the HSTs have different mode of actions, biochemical reactions, and signaling mechanisms to causes diseases in the host plants. These HSTs have devastating effects on host plant tissues by affecting biochemical and genetic modifications. Host-specific mycotoxins such as AK-toxin, AF-toxin, and AC-toxin have the devastating effect on plants which causes DNA breakage, cytotoxic, apoptotic cell death, interrupting plant physiology by mitochondrial oxidative phosphorylation and affect membrane permeability. This article will elucidate an understanding of the disease mechanism caused by several Alternaria HSTs on host plants and also the pathways of the toxins and how they caused disease in plants.

Keywords: 1O2, singlet oxygen; AA, ascorbic acid; ALT, alternuene; AME, alternariol 9-monomethyl ether; AOH, alternariol; APX, ascorbate peroxidase; ATX, alterotoxin; Alternaria species; CAT, catalase; CDCs, conditionally dispensable chromosomes; DHAR, dehydroascorbate reductase; DHT, dihydrotentoxin; GPX, guaiacol peroxidase; GR, glutathione reductase; GSH, glutathione; H2O2, hydrogen peroxide; HR, hypersensitive response; HSTs, host specific toxins; Host-specific toxins; MDHAR, monodehydroascorbate reductase; NO, nitric oxide; NRPS, nonribosomal peptide synthetase; Non-host-specific toxins; O2˙ˉ, superoxide anion; PCD, programmed cell death; PKS, polyketide synthase gene; Pathogenicity; REMI, restriction enzyme-mediated integration; ROS, reactive oxygen species; SMs, secondary metabolites; SOD, superoxide dismutase; Secondary metabolites; TEN, tentoxin; TeA, tenuazonic acid; UGT, UDP-Glucuronosyltransferases; nHSTs, non-host specific toxins; ˙OH, hydroxyl radical.

Graphical abstract

Fig. 1

Schematic presentation of target sites of HSTs produced by Alternaria species. Ch: chloroplast, ER: endoplasmic reticulum, GA: Golgi apparatus, Mt: mitochondrion, Nu: nucleus, Pd: plasmodesma, Pm: plasma membrane, Vc: vacuole.

Fig. 2

Chemical structures of host-specific toxins produced by various species of Alternaria (Modified of [4]).

Fig. 3

Schematic presentation of sphingolipids metabolism pathways and consequences of S1P lyase deficiency, and also presents the site of AAL-toxin/fumonisin inhibition. S1P lyase paucity leads to enhance of cellular S1P and sphingosine (to a smaller extent). Thus, de novo sphingolipid biosynthesis (blue arrows) is decreased may be up-regulation of Orm1/3 expression. At the same time, the recycling pathway (gray arrows) is elevated. SMS: sphingomyelin synthases, SMase: sphingomyelinases, CS: ceramide synthases, CDase: ceramidases, SPP: S1P phosphatase, SK: sphingosine kinases.

Fig. 4

Summary through the diagrammatic presentation of the mode of actions of AK-, ACR- and AM-toxins in susceptible plants.

Fig. 5

Role of ROS when pathogen attack situation (↑ represents up-regulation of ROS production, whereas represents down-regulation of ROS scavenging mechanisms). ROS play multifaceted action. The most important ROS-induced mechanisms during plant-pathogen interaction are peroxidase- and ROS-induced cross-linking of cell wall components which play an important role in the defense mechanisms against the pathogens. Furthermore, a defence-induced PCD, known as HR is stimulated and organized by the intricate crosstalk between ROS and RNS. In conclusion, ROS can be transform several other multiple signaling pathways and cell to cell reactions persuaded by various biotic and abiotic stimuli, by the oxidation-dependent regulation of transcription factors and by the co-induction and co-regulation of the secondary messenger Ca²⁺. PCD: programmed cell death, ROS: reactive oxygen species, RNS: reactive nitrogen species, H₂O₂: hydrogen peroxide, O₂^‾: superoxide radicals, HR: hypersensitive response. *Note: For more information about the role ROS see review, Apel and Hirt [180].