Just how many types of filamentous phytopathogens are there? Catastrophy for the bio/hemi/necrotroph divisions

James Hane 1 Jonathan Paxman 1 Darcy Jones 1 Alison Testa 1 Richard Oliver 1 Pierre de Wit 2
1CCDM, Curtin University, Perth, Australia
2Phytopathology, Wageningen University, Wageningen, Netherlands

The classification model that has dominated fungal plant pathology for the last 50 years is that diseases and pathogens can be divided into three ‘trophic’ classes, biotroph, hemibiotroph and necrotroph. Non-pathogen species are described as a symbiont when they live on or within a living host without causing significant damage or as saprotrophs when they extract nutrients solely from decaying biomaterials.

This model of pathogen classification leaves much to be desired. Many pathogens are placed by different authors in two or even all three of these classes. Apart from the undisputed fact that all obligate pathogens are all biotrophic, no phenotypic feature can be described as diagnostic. Other pathogens, such as the wilts and those causing root diseases do not obviously comply with the biotroph/hemi/necrotroph trichotomy.

There are now 642 fungal and oomycete species with genome sequences of which 137 are pathogens. We set out to determine whether an objective analysis of these genomic resources could provide a robust classification system with predictive power.

We developed a technique for the assessment of trophic phenotypes just using the gene content of carbohydrate active enzymes (CAZyme). We found that the existing tripartite trophic classification system for is unsustainable. Instead our analysis identified novel clusters comprising eight pathogen trophic descriptors and a saprobe trophic class. These are -1- haustorial biotroph (BH), -2- non-haustorial biotroph (BN), -3- biotroph/symbiont (BS), -4- intracellular hemibiotroph (HI), -5- extracellular hemibiotroph (HE), -6- broad host range necrotrophs (NB), -7- narrow host range necrotrophs (NN) and finally -8- the wilts, anthracnoses and rots (WAR). This study highlights some longstanding anomalies and permits the objective prediction of properties of a species based solely on its CAZyme gene content. We have used the data included in this study to develop and train a predictive tool for CAZyme-Assisted Training And Sorting of TROPHY which we call CATASTROPHY.