Elsinoë fawcettii and Elsinoë australis: the fungal pathogens causing citrus scab

Abstract

Elsinoë fawcettii and E. australis are important pathogens of citrus. Both species are known to produce red or orange pigments, called elsinochrome. Elsinochrome is a nonhost-selective phytotoxin and is required for full fungal virulence and lesion formation. This article discusses the taxonomy, epidemiology, genetics and pathology of the pathogens. It also provides a perspective on the cellular toxicity, biosynthetic regulation and pathological role of elsinochrome phytotoxin.

Taxonomy: Elsinoë fawcettii (anamorph: Sphaceloma fawcettii) and E. australis (anamorph: S. australis) are classified in the Phylum Ascomycota, Class Dothideomycetes, Order Myriangiales and Family Elsinoaceae.

Host range: Elsinoë fawcettii causes citrus scab (formerly sour orange scab and common scab) on various species and hybrids in the Rutaceae family worldwide, whereas E. australis causes sweet orange scab, primarily on sweet orange and some mandarins, and has a limited geographical distribution.

Disease symptoms: Citrus tissues infested with Elsinoë often display erumpent scab pustules with a warty appearance. TOXIN PRODUCTION: Elsinochrome and many perylenequinone-containing phytotoxins of fungal origin are grouped as photosensitizing compounds that are able to absorb light energy, react with oxygen molecules and produce reactive oxygen species, such as superoxide and singlet oxygen. Elsinochrome has been documented to cause peroxidation of cell membranes and to induce rapid electrolyte leakage from citrus tissues. Elsinochrome biosynthesis and conidiation are coordinately regulated in E. fawcettii, and the environmental and physiological inducers commonly involved in both processes have begun to be elucidated.

Figure 1

Disease cycle of citrus scab caused by Elsinoë fawcettii on fruit, twigs and leaves, showing corky lesions with erumpent scab pustules.

Figure 2

Accumulation of red‐ or yellow‐pigmented elsinochrome phytotoxin by the isolates of Elsinoë fawcettii. The fungal cultures were grown on potato dextrose agar in the light for 4 weeks. The chemical structures and tautomer of elsinochrome (1,2‐dihydrobenzo‐perylenequinone) A–D are also shown.

Figure 3

(a) Thin‐layer chromatography (TLC) analysis of elsinochrome produced by Elsinoë fawcettii, causing citrus scab. Elsinochrome was separated on silica gel using a solvent containing chloroform and ethyl acetate (1 : 1, v/v). (b) Induction of necrotic lesions on citrus leaves treated with elsinochrome (ESC). The mock controls were treated with acetone alone.

Figure 4

Schematic diagram showing the elsinochrome (ESC) biosynthetic gene cluster with predicted functions identified in Elsinoë fawcettii. This figure shows data reprinted from fig. 1 of Chung and Liao (2008) [reprinted with permission from the Society for General Microbiology (UK)].

Figure 5

Proposed biosynthetic pathway and involvement of the gene products leading to the formation of elsinochrome and conidia by Elsinoë fawcettii.

Figure 6

Proposed regulatory pathways involving two transcriptional activators, TSF1 and EfSTE12, and leading to the production of elsinochrome (ESC) and conidia in Elsinoë fawcettii. On exposure to light, ESC assumes an activated triplet state which reacts with oxygen to produce superoxide (O₂ ^·−) through a reducing substrate (R) or singlet oxygen (¹O₂) via an energy relay reaction. A cross indicates an inhibitory effect for ESC biosynthesis, presumably by blocking the expression of TSF1 and thus of the elsinochrome‐biosynthetic genes. A filled rectangle indicates the inhibitory activity of expression of the ESC biosynthetic genes. TSF1 is also required for conidiation. The regulation of ESC biosynthesis by EfSTE12 bypasses TSF1 and is probably controlled by a mitogen‐activated protein kinase (MAPK)‐mediated signalling pathway.