Kasuga Takao, Bui Mai, Bernhardt Elizabeth, Swiecki Tedmund, Aram Kamyar, Cano Liliana M, Webber Joan, Brasier Clive, Press Caroline, Grünwald Niklaus J, Rizzo David M, Garbelotto Matteo
Crops Pathology and Genetics Research Unit, USDA Agricultural Research Service, Davis, California, 95616, USA.
Phytosphere Research, Vacaville, California, 95687, USA.
BMC Genomics. 2016 May 20;17:385. doi: 10.1186/s12864-016-2717-z.
Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.
We show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.
This work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival.
非整倍体可导致显著的表型变化，有时这种变化具有选择性优势。例如，非整倍体赋予人类致病真菌对抗真菌药物的抗性。在野外，侵袭性真菌和卵菌植物病原体中也观察到了非整倍体现象。有利于非整倍体产生的环境、潜在的遗传机制以及非整倍体对侵袭性的贡献尚未得到充分研究。我们研究了樟疫霉的表型多样化及相关的基因组变化，樟疫霉是一种极具破坏性的卵菌病原体，宿主范围广泛，在北美西部导致橡树猝死，在英国导致落叶松猝死。该病原体的引入种群完全是克隆性的。在加利福尼亚州，从树干溃疡病中分离得到的橡树（栎属物种）分离株经常表现出宿主依赖性的非典型表型，称为非野生型（nwt），显然没有任何宿主相关的种群分化。基于对来自不同宿主的基因型的大规模调查，我们之前推测橡树溃疡病中的环境可能是樟疫霉中观察到的表型多样化的原因。
我们发现，当从人工接种的峡谷活橡树（金黄栎）的溃疡病中重新分离来自叶宿主加利福尼亚月桂树（加州月桂）的野生型樟疫霉分离株时，可获得正常野生型（wt）和nwt表型。我们还在英国劳森柏（美国扁柏）树皮溃疡病的樟疫霉分离株中发现了类似的nwt表型；此前在该病原体种群中未知nwt的存在。基于高通量测序的分析确定了主要的基因组改变，包括主要在nwt分离株中的部分非整倍体和杂合性的拷贝中性缺失。染色体断点位于转座子处或其附近。
这项工作表明病原体的主要基因组改变可由其宿主物种诱导。这是一种未被记录的植物 - 微生物相互作用类型，其对病原体进化的贡献尚待研究，但nwt表型的潜在附带效应之一可能是宿主存活。
