Dynamic Extreme Aneuploidy (DEA) in the vegetable pathogen Phytophthora capsici sheds light on instant evolution and intractability

Abstract

word summaryOomycete plant pathogens are notoriously difficult to control, and individual isolates are highly unstable; making routine research challenging. Sequencing reveals extreme aneuploidy for single-spore progeny of the vegetable pathogen Phytophthora capsici; a phenomenon dubbed Dynamic Extreme Aneuploidy (DEA). Although extreme, the aneuploidy appears to be moderately stable. A single sporulating plant lesion may produce an armada of genetically unique individuals and helps explain the rapid increase of advantageous alleles (e.g. drug resistance), mating type switches to allow sex and the widely observed phenomenon, loss of heterozygosity (LOH). Investigation of other oomycetes indicate this phenomenon is not unique to P. capsici. Dynamic Extreme Aneuploidy (DEA) in the vegetable pathogen Phytophthora capsici sheds light on instant evolution and intractability. Introductory ParagraphAlthough oomycete plant pathogens (water molds) look and act like fungi, they are distantly related and most antifungal compounds have no effect 1 . Oomycetes are notoriously difficult to control 2-4 . In research, isolates are highly unstable; making routine research challenging 5,6 . Here we show that ploidy amongst the chromosomes in an individual isolate varies dramatically for asexual spores of Phytophthora capsici; a phenomenon dubbed Dynamic Extreme Aneuploidy (DEA). The number of individual chromosomes allocated to a single zoospore is highly variable and appears moderately stable. The practical consequence is that infected plants can release an armada of genomically unique individuals -responding quickly to selection pressures. DEA explains the rapid increase of advantageous alleles (e.g. drug resistance) 7 , mating type switches to allow sex and loss of heterozygosity (LOH) 8-10 and may spur novel investigation of yeast and human tumor tissues where loss of heterozygosity is reported 11,12 .The genus Phytophthora has many destructive and pervasive plant pathogens 2 . The 120+ species attack almost all dicot plants and threaten ecosystems and entire plant industries 2,4 . For more than 150 years, scientists have struggled to manage this unwieldy genus and make of it (or, at least one of its members) a model organism 13 . Part of this quest has focused on the vegetable pathogen, P. capsici -a devastating pathogen of vegetables [13][14][15] . Ostensibly, an ideal research model; isolates can be immortalized under liquid nitrogen, grow rapidly on simple media, can be easy to mate in the laboratory, are often highly pathogenic and make copious spores with little coaxing. The problem is -sometimes an isolate will do all the above and sometimes it won't. The intractability of Phytophthora (or success, depending on your point of view) lies in its plasticity 5 . Phytophthora, when needed most (e.g. for a long-term laboratory, greenhouse or field experiments), is entirely unreliable.The ploidy of oomycetes was debated actively for over 75 years and it wasn't until Eva Sansome, in a 1961 Letter to Nature, provided convincin...

A Double-Edged Sword: Aneuploidy is a Prevalent Strategy in Fungal Adaptation

“…Recently, sequencing of the single-spore isolates of a vegetable pathogen Phytophthora capsica revealed heterogeneous, drastic, and stable aneuploidy. This dynamic, extreme aneuploidy was speculated to confer observed resistance to mefenoxam, a commonly used phytopathogenic toxin [100]. In contrast, in isolates of the sudden oak death pathogen Phytophthora ramorum , aneuploid isolates exhibited slower growth and lower pathogenicity compared to wild-type isolates, reiterating the dichotomous nature of aneuploidy in host-pathogen interactions [101].…”