Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution

Abstract

Chemical defences represent a main trait of the plant innate immune system. Besides regulating the relationship between plants and their ecosystems, phytochemicals are involved both in resistance against pathogens and in tolerance towards abiotic stresses, such as atmospheric pollution. Plant defence metabolites arise from the main secondary metabolic routes, the phenylpropanoid, the isoprenoid and the alkaloid pathways. In plants, antibiotic compounds can be both preformed (phytoanticipins) and inducible (phytoalexins), the former including saponins, cyanogenic glycosides and glucosinolates. Chronic exposure to tropospheric ozone (O(3)) stimulates the carbon fluxes from the primary to the secondary metabolic pathways to a great extent, inducing a shift of the available resources in favour of the synthesis of secondary products. In some cases, the plant defence responses against pathogens and environmental pollutants may overlap, leading to the unspecific synthesis of similar molecules, such as phenylpropanoids. Exposure to ozone can also modify the pattern of biogenic volatile organic compounds (BVOC), emitted from plant in response to herbivore feeding, thus altering the tritrophic interaction among plant, phytophagy and their natural enemies. Finally, the synthesis of ethylene and polyamines can be regulated by ozone at level of S-adenosylmethionine (SAM), the biosynthetic precursor of both classes of hormones, which can, therefore, mutually inhibit their own biosynthesis with consequence on plant phenotype.

Keywords: phytoalexins; phytoanticipins; phytochemicals; secondary metabolism; stress physiology; tropospheric ozone pollution; volatile organic compounds.

Figure 1.

Stressor dose-stress effect relationships in plants.

Figure 2.

Main classes of alkaloid precursors and derivatives (the example number refers to the corresponding alkaloid class).

Figure 3.

Beneficial and detrimental pools of ozone in the stratosphere and troposphere, respectively. In the stratosphere this pool is depleted by fluorochlorocarbons (CCl₂C₂) while in the troposphere it is raised by photochemical smog.

Figure 4.

Relationships between ozone and herbivorous-induced BVOCs and their influence on photochemical ozone precursors and on tritrophic interactions, respectively.

Figure 5.

Influence of different stresses on plant metabolism. The activation of induced resistance leads to the accumulation of numerous defence compounds that may unbalance the equilibrium between primary and secondary metabolism, thus resulting in fitness costs for the plant. On the other hand, the synthesis of secondary metabolites due to a stress may protect plant from other different stresses.

Scheme 1.

Aromatic amino acid biosynthesis from shikimate and phenyl-alanine derivatives of the phenylpropanoid pathway. Depending on the species and the conditions (i.e., during pathogen attack) salicylic acid can also be synthesized from chorismate.

Scheme 2.

Main steps of the phenylpropanoid pathway leading to benzoic acids, hydroxycinnamates (coumaric, ferulic and sinapic acids) and lignin, (CA4H, cinnamate-4-hydroxylase; C3H, coumarate-3-hydroxylase; CAD, cinnamyl alcohol dehydro-genase CCR, cinnamoyl: CoA reductase; CL, 4-Coumarate: CoA ligase; PAL, phenylalanine ammonia-lyase.

Sckeme 3.

Isoprenoid pathway from acetyl-CoA. The enzyme with an asterisk is reported to be influenced by ozone.

Scheme 4.

Molecular structures of the major oat and tomato saponins (adapted from Osbourn, [32]).

Scheme 5.

Generation of hydrocyanic acid from a cyanogenic (HCN) glucoside precursor. The α-hydroxynitrile intermediate is then converted by α-hydroxynitrile lyase to HCN and aldehyde or ketone.

Scheme 6.

Hydrolysis of glucosinolates and degradation of the unstable aglycone to isothiocyanates, nitriles and athiocyanates.

Scheme 7.

Schematic biosynthetic pathway of camalexin via indole-3-acetoaldoxime. Other important indolic compounds arise from the same route.

Scheme 8.

Involvement of S-adenosylmethionine (SAM) in polyamine and ethylene biosynthesis. The metabolic shift to ethylene or polyamine biosynthesis can enhance ozone susceptibility or tolerance, respectively.