#068: Frosty Pod Rot Disease of Cacao Trees

Frosty Pod Rot, caused by the fungus Moniliophthora roreri, is one of the most significant pathogens of cacao trees (Theobroma cacao). The disease has been around a long time: it was first recognized in Ecuador in 1917 and first described in 1933.  roreri likely evolved in Columbia, where the greatest diversity of the species is located and where cultivated cacao trees grow near closely related trees.  Up until the 1950’s, Frosty Pod Rot was limited to northwestern South America.  Since then, it has spread throughout Central America and into Peru and Venezuela.  In these areas, Frosty Pod Rot is the most destructive cacao disease, resulting in the loss of about 30-40% of total production.  The disease has not yet made it to Asia or Africa, where most of the world’s chocolate is produced, but it may just be a matter of time.

Frosty Pod Rot has a fairly simple life cycle.  It can only infect actively growing seed pods produced by trees in the closely related genera Theobroma and Herrania.  A fungal spore lands on a seed pod, germinates, and grows inside the pod.  Infected pods appear more yellow than normal and are sometimes slightly misshapen.  Older pods ripen early and are noticeably heavier than healthy pods.  Inside, the beans in the infected area appear watery, brown (they should be white at this stage), and necrotic (dead).  Eventually, the pods develop dark brown lesions that expand to cover the entire seed pod.  These lesions are soon covered in off-white, felty fungal hyphae.  It is this part of the disease’s progression which gives Frosty Pod Rot its common name.  These external hyphae release spores into the air, infecting new hosts.  The entire seed pod eventually dies and withers, but does not drop from the tree.  During this time, hyphae grow over the rest of the pod surface and the dead pod becomes a spore factory.  The hyphae slowly turn yellow as the fungus uses up the remaining nutrients in the withered pod.

Although Frosty Pod Rot does not harm the tree itself, infected pods are completely lost.  How much of the cacao crop is lost varies by region.  In areas with a dry season of four months or more, such as the Machala region in Ecuador, about 20-30% of annual yields are lost.  In areas characterized by year-round rain and high temperatures, such as Atlantic Costa Rica, annual yields are reduced by as much as 80-90%.  Losses in Columbia average 30-40% and those in Peru average 40-50%.  Local losses can vary greatly, with some farms losing 100% of their crop.  These unlucky farms must be abandoned in favor of profitable crops.  Currently, the only things keeping the fungus from infecting the entire world’s cacao trees are the oceans on either side of the Americas.  Frosty Pod Rot spores can survive for up to nine months, so accidental transportation by humans is a primary concern in the spread of this disease.  For now, anyway, there are greater pressures affecting chocolate supply, such as greater demand from China and greater demand for dark chocolate.  Despite everything, in November the International Cocoa Organization assured everyone that there will be enough chocolate to meet the world’s demand for the foreseeable future.

The primary way in which Frosty Pod Rot is treated is the removal of infected seed pods.  In order to prevent further infection, this must be done before the fungus breaks the surface and produces spores.  Farmers can tell if a pod is infected a week before the fungus produces spores, but this is pod-by-pod examination is time-consuming and therefore not cost-effective.  There are currently no cost-effective fungicides that treat Frosty Pod Rot, so farmers cannot use any traditional disease management techniques.  Current efforts are focused on preventing the spread of Frosty Pod Rot, mainly through quarantine practices.  Recently, people have begun to research alternative methods to control Frosty Pod Rot.  One approach that has the potential to help uses endophytic fungi to protect the tree against Frosty Pod Rot.  These fungi grow inside the tree without harming it, so they are perfectly positioned to combat the disease.  Unfortunately, much more research will be required before endophyte-mediated resistance can be used on a large scale.  Another area of research is trying to develop cacao trees that are resistant to Frosty Pod Rot.  Currently, no cacao varieties are resistant to the disease.  Theobroma cacao evolved in the Amazon, but was first cultivated in Central America.  Cultivated cacao trees were therefore free of natural pathogens and did not retain resistance to diseases like Frosty Pod Rot.  There are some varieties that are slightly less susceptible, particularly those that produce pods during the dry season.  These natural variations will have to be greatly scaled up before they are able to reduce disease incidence.

M. roreri is a very bizarre fungus. Don’t be fooled by the description above: it is not an average mold. If you think it sounds like an everyday mold, you’re not alone.  The mycologists who first classified the fungus grouped it with a bunch of average molds in the phylum Ascomycota.  None of these ascomycetes produced sexual spores, and it was clear that “Monilia” roreri only produced conidia (asexual spores).  This seemed like a good fit for the species until 1978, when someone noticed that the hyphae of M. roreri had doliopore septa, which are only found in fungi from the phylum Basidiomycota.  It was then placed in its own genus Moniliophthora, but no one was sure where it should go within the Basidiomycota.  Eventually, people noticed similarities between M. roreri and another cacao disease, Crinipellis perniciosa (Witch’s Broom Disease of cacao, FFF#113).  The two cacao pathogens produce similar infection structures, have a similar hyphal morphology, and have similar spore formation pathways.  However, there was one major difference between the two: C. perniciosa produced sexual spores on mushrooms.  C. perniciosa made small, reddish, parasol-shaped mushrooms.  The distinctive shape of these mushrooms placed it within the family Marasmiaceae, most of which are non-pathogenic decomposers.  Modern genetic techniques demonstrated that M. roreri was, in fact, closely related to C. perniciosa.  Genetic studies also revealed that C. perniciosa was more closely related to M. roreri than either was to the rest of the fungi in the genus Crinipellis.  Today, both of these pathogens are placed in the genus Moniliophthora, which belongs to the Marasmiaceae.

But the unusual features of M. roreri do not end with taxonomical uncertainty.  As it turns out, the initial assessment that M. roreri only produces asexual cells is not true.  Detailed studies of M. roreri spores have shown that its “conidia” function as sexual spores.  Since conidia are defined as strictly asexual spores, mycologists will probably have to come up with a new name for these strange spores.  Currently, M. roreri is the only member of the order Agaricales (gilled mushrooms) to exhibit this unusual spore behavior.  The theory explaining these spores suggests that they are produced on highly modified basidia (sexual cells of the Basidiomycota).  For some reason, the basidia evolved to be thin and produce spores in chains as if they were asexual conidiophores.  Using this theory, it follows that the felty tissue produced on the exterior of seed pods is a highly reduced pileus (the cap of a mushroom).

What could cause the fungus to abandon the gilled mushroom shape in favor of a highly reduced structure?  M. roreri produces many, many more spores than its close relative, M. perniciosa.  Most fungi increase spore production by producing larger or more mushrooms, since gills efficiently pack a large surface are into a small space.  M. roreri, however, clearly values spore number over packing efficiency.  I suspect that M. roreri lost its mushrooms because the pod on which it grows already provides a large, stable surface from which the fungus can drop spores into air currents.  Without having to produce mushrooms, more resources can be devoted to spore formation.  Its spores are also designed to survive long periods of adverse conditions.  Old spores develop thick walls and become darker, which allows them to survive for longer periods of time than the pale, thin-walled spores produced by M. perniciosa.  One theory explaining these characteristics suggests that M. roreri was cut off from its main host population when the Andes formed.  The remaining host species were probably widely scattered throughout the forests, so M. roreri had to produce a great number of spores that could survive long periods of time in adverse conditions in order to successfully infect plants over a long distance.  It is because of these ancient selective pressures that the fungus is such a successful pathogen in the Americas.  Due to the sheer number of spores produced by M. roreri and its ability to thrive in a variety of environments, farmers have found it impossible to stop the spread of Frosty Pod Rot.

If you’re interested in the production of chocolate, see FFF#024.

See Further:

http://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsid=34779

http://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-97-12-1640

http://www.slate.com/blogs/moneybox/2014/11/24/chocolate_crisis_fears_of_a_cocoa_shortage_may_be_overblown.html

http://blogs.scientificamerican.com/artful-amoeba/2013/08/14/chocolate-frosty-pod-rot-and-you/

http://users.aber.ac.uk/gwg/pdf/griffith-wbdbiologist.pdf

http://www.mycologia.org/content/97/5/1012.full

http://www.agriculture.gov.tt/images/tips/Frosty-pod-rot-cocoa.pdf