fungi go bananas

Plant pathologists have a sense of mission.  Take Ioannis Stergiopoulos.  Professor Stergiopoulos studies sigatoka disease of banana.  In case you are inclined to dismiss bananas as just a snack food, Stergiopoulos is ready point out that bananas are one of the top five staple crops in the world.  However, because they are clonally propagated, the world banana crop is dominated by a single variety and thus particularly vulnerable to potential emerging diseases.  Stergiopoulos also points out that pathogenic fungi in general are an emerging threat as they evolve new virulence genes.


Sigatoka is a complex of three diseases caused by closely related fungi.  Yellow sigatoka, caused by the fungus Pseudocercospora musae (P. musae for short), has been known for over a century.  Black sigatoka, caused by P. fijiensis, was discovered in 1963.  Eumusae leaf spot, caused by P. eumusae, was discovered the most recently, in the mid-1990s.  There is a progression of aggressiveness in the three species.  When black sigatoka arrives in a country that has only yellow sigatoka, it effectively displaces it, and then eumusae does the same with black sigatoka.  Black sigatoka can infect banana cultivars that are resistant to yellow sigatoka, and eumusae can infect cultivars resistant to sigatoka of either color (technically, to satisfy the plant pathologists, it is the pathogen that does the infecting, e.g. P. musae, and the disease is the result, e.g. yellow sigatoka; I will use “black sigatoka” as an abbreviation for “the black sigatoka pathogen”, etc.).  And while black sigatoka currently causes the biggest yield losses of the three, eumusae, which has not yet encircled the globe, is in a class with black sigatoka in terms of virulence.


Where do such diseases come from?  Stergiopoulos addresses that question using his extensive tool kit of genomic techniques, with which he can look at all the DNA that each species possesses and dig out trends in the genes.  His team analyzed mutations in 46 genes that are common to all species in the class of fungi that the three pathogens belong to, genes that seem to be important enough that they evolve very slowly.  This analysis showed that while the three belong to a single lineage, black sigatoka branched off first, while the other branch gave rise to yellow sigatoka and eumusae later.  They then looked at the family tree of these three plus other members of the class (remember that a class contains many orders and an order contains many families — maybe that would make it a class tree?) and overlaid the tree on the timeline from the first appearance of the class in geologic time in order to date the branches.  Black sigatoka branched off between 30 and 40 million years ago, while the other branch split into yellow sigatoka and eumusae lineages between 17 and 23 million years ago.  So not only does black sigatoka predate yellow, the reverse of their appearance in banana plantations, but all three predate the 20th century by more than a little.  So why the delay?


Of course there were probably other lineages that were branching off all this time — why should only these three species have become pathogenic?  Quite likely they were not pathogenic or else possessed little virulence when they first split off.  Pathogens have to acquire or adapt genes that let them take advantage of hosts.  Stergiopoulos’ analysis is able to give an idea of just how.


The three species’ genomes were found to contain a large proportion of transposable elements.  These are strings of DNA that contain genes that will copy the information in their own DNA string to another place in the genome.  This kind of random opportunistic jumping of segments of DNA to new sites tends to play havoc with the existing set of genes, but it can also occasionally cause advantageous outcomes.  The transposable elements can cause duplication of various genes, and sometimes the duplicate genes can evolve to take on new functions.


For a fungus to be a pathogen at all, it has to overcome a host plant’s defenses.  It does this with proteins called effectors, which disable components of the plant’s defense system.  A fungus can have the genes to produce a suite of different effectors, each one capable of taking on a different strategy that the plant can muster.  An expanded suite of effectors that can each evolve individually can be to the fungus’ advantage.  Stergiopoulos’ team found over 100 genes in each of the three sigatoka pathogens that show the genetic signature of effectors, and for each species about half of these genes arose after the lineages separated, quite possibly through evolution of duplicated effector genes.  Every time one of these effectors evolves to a point where it knocks out a host defense, the fungus gains an incremental advantage in growing and reproducing at the plant’s expense.


A pathogen also needs to be able to use the host’s resources for its own growth and reproduction.  A key aspect of this resource hijacking is the ability to digest the host’s cell walls.  The team found that black sigatoka and eumusae have had duplications of many of the same genes used for cell wall digestion, and this was a result of pure coincidence.  This parallel evolution is in some sense an adaptation to the host plant.  An increase in virulence afforded by enhanced cell wall digesting ability could also allow the fungi to grow and spread more easily, which we would then come to our attention as an emerging disease.


The team wanted to know what other genes might be different between yellow sigatoka on the one hand and the more virulent species on the other, in order to get a fuller picture of the traits that make a fungus more virulent.  They compared the three species’ genes to annotated lists of genes of known function in all eukaryotes (plants, animals, fungi, protozoans, etc.), paying special attention to genes that had gotten duplicated.  The result that popped out was an increase in copies in black sigatoka and eumusae of genes associated with metabolism — genes for transport and metabolism of amino acids, fats, carbohydrates, and secondary metabolites and genes for energy use.  Since the two species have achieved higher virulence, the team believes that an increase in pathways for metabolism is key for virulence.  One could imagine that when cell-wall-digesting enzymes liberate a plant cell’s juices, a fungus that has greater capacity for handling the spoils would insure that more of the goodies go toward its own growth and reproduction, rather than letting nearby opportunistic fungi take advantage of them.


Thus, the Stergiopoulos team has done a magnificent job of presenting the How of the evolution of virulence — gene duplications, evolution of effectors, increased ability to digest cell walls, and increased capacity to use the resources liberated.  What is outside of their purview is the Why.  Why should three species that have been evolving for millions of years all turn virulent in the 20th century?  Researchers who love mining genomes for scientific treasures will use plant pathogens as prospecting grounds, and they will justify their intellectual pursuits to funding agencies by promising insights into developing targeted disease control methods.  Meanwhile the environmental and economic factors that lead to the emergence of new pathogens are no secret to molecular plant pathologists, but they are just not as interesting to people attracted to the minutiae of genetic information.


And what are these factors?  Environmental factors include monocropping, sequential cropping of the same species, low genetic diversity, and movement of plant material across continents and oceans, all the product of human intervention.  Bananas are a special case, being sterile triploids that present problems for breeding, and being propagated from side shoots that can be planted across fields and countries leading to essentially one big banana plant with zero diversity divided up into multiple stalks across the landscape.  When a fungus can grow unimpeded over a vast area year after year, every cell division and every mating is an opportunity to evolve to better take advantage of a plentiful host.  When infected material is transported by long-distance travelers, a previously unknown disease from the Sigatoka District of Fiji can end up with a worldwide distribution.


However, many of the factors underlying the environmental are the economic.  Corporations seeking to make money selling a product find an agricultural commodity that is easy to produce, tolerates long-distance shipping, and presents a uniform quality that shoppers expect on supermarket shelves, they plant it in machine-harvestable rows at the maximum density, they fertilize it into a succulent treat for a fungus, and they promote it in extensive advertising campaigns that make an exotic tropical fruit seem like a necessary addition to a bowl of cereal in a country without a banana industry.  The profit motive overrides environmental and phytopathological considerations.


With this backdrop, the efforts of molecular plant pathologists can actually serve to consolidate corporate dominance of agriculture.  Moneyed interests recruit scientists to find high-investment technologies that will favor the biggest growers.  Plant pathologists deceive themselves into believing they are feeding the world, when they are actually propping up corporate profits, leaving the hungry still hungry.  Even the claim of saving a widely grown staple crop is equivocal, with a significant portion of the world harvest being industrially produced by multinational corporations for export.


We need scientists who are experts on plant diseases who can aid us in diagnosing our crops, advise us on designing our agroecosystems, assist our efforts in harnessing crop evolution, and warn us about emerging threats.  But when food becomes a commodity, scientific expertise becomes captured and misdirected.  What would an economic system look like where food is not a commodity?  It will take many minds to work out all the details, but it probably will not include a banana on your daily bowl.

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