Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao: what's new from this old foe?

Abstract

Moniliophthora perniciosa (=Crinipellis perniciosa) causes one of the three main fungal diseases of Theobroma cacao (cacao), the source of chocolate. This pathogen causes Witches' broom disease (WBD) and has brought about severe economic losses in all of the cacao-growing regions to which it has spread with yield reductions that range from 50 to 90%. Cacao production in South America reflects the severity of this pathogen, as the yields in most of the infected regions have not returned to pre-outbreak levels, even with the introduction of resistant varieties. In this review we give a brief historical account and summarize the current state of knowledge focusing on developments in the areas of systematics, fungal physiology, biochemistry, genomics and gene expression in an attempt to highlight this disease. Moniliophthora perniciosa is a hemibiotrophic fungus with two distinct growth phases. The ability to culture a biotrophic-like phase in vitro along with new findings derived from the nearly complete genome and expression studies clearly show that these different fungal growth phases function under distinct metabolic parameters. These new findings have greatly improved our understanding of this fungal/host interaction and we may be at the crossroads of understanding how hemibiotrophic fungal plant pathogens cause disease in other crops.

Historical summary of wbd: The first WDB symptoms appear to have been described in the diaries of Alexandre Rodrigues Ferreira (described as lagartão; meaning big lizard) from his observations of cacao trees in 1785 and 1787 in Amazonia, which is consistent with the generally accepted idea that M. perniciosa, like its main host T. cacao, evolved in this region. The disease subsequently arrived in Surinam in 1895. WBD moved rapidly, spreading to Guyana in 1906, Ecuador in 1918, Trinidad in 1928, Colombia in 1929 and Grenada in 1948. In each case, cacao production was catastrophically affected with yield reductions of 50-90%. After the arrival of M. perniciosa in Bahia in 1989, Brazil went from being the world's 3rd largest producer of cacao (347 000 tonnes in 1988-1990; c. 15% of the total world production at that time) to a net importer (141 000 tonnes in 1998-2000). Fortunately for chocolate lovers, other regions of the world such as West Africa and South East Asia have not yet been affected by this disease and have expanded production to meet growing world demand (predicted to reach 3 700 000 tonnes by 2010).

Classification: Moniliophthora perniciosa (Stahel) Aime & Phillips-Mora: super-kingdom Eukaryota; kingdom Fungi; phylum Basidiomycota; subphylum Agaricomycotina; class Agaricomycetes; subclass Agaricomycetidae; order Agaricales; family Marasmiaceae; genus Moniliophthora.

Useful websites: http://www.lge.ibi.unicamp.br/vassoura/, http://nt.ars-grin.gov/taxadescriptions/keys/TrichodermaIndex.cfm, http://www.worldcocoafoundation.org/info-center/research-updates.asp, http://www.ars.usda.gov/ba/psi/spcl.

Figure 1

WDB disease in the field. (A) An infected cacao grove in Bahia, Brazil. (B) An uninfected cacao grove in Bahia, Brazil. (C) Infected tree with WBD symptoms of dry brooms, parthenocarpic fruits and an infected pod. The ovals with the white dashed lines represent dry brooms. The ovals with the solid white lines show parthenocarpic fruits. The white arrow points to a diseased pod. (D) Infected tree with WBD symptoms with a single dry broom. The oval with the dashed white line encircles the dry broom.

Figure 2

Basidiocarps and pod rots resulting from M. perniciosa infection of cacao. (A) Basidiocarps on a dry broom at various development stages. (B) A basidiocarp on a dry broom after spore release. The white arrow shows the accumulation of the spores on the dry broom. (C) Basidiocarp development on a dry broom in the field. (D) Pod rot caused by M. perniciosa. Longitudinal view. (E) Pod rot caused by M. perniciosa. Transverse view.

Figure 3

Disease progression (left to right). The images of the fungal stage above represent the progression of the fungus from the biotrophic phase to the saprotrophic phase and the typical mycelial structures and nuclei number at each symptomatic stage shown below. (A) Infection by penetration through stomatal opening. (B) Growth of the green broom. (C) Necrosis of infected tissues. (D) Dry broom. (E) Basidiocarp and spore formation.