The Sainsbury Laboratory, Norwich Research Park, Colney Ln, Norwich, NR4 7UH, UK.
Graduate School of Agricultural Science, Kobe University, Kobe, Japan.
BMC Evol Biol. 2018 Jul 5;18(1):93. doi: 10.1186/s12862-018-1201-6.
Outbreaks caused by asexual lineages of fungal and oomycete pathogens are a continuing threat to crops, wild animals and natural ecosystems (Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ, Nature 484:186-194, 2012; Kupferschmidt K, Science 337:636-638, 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl MF, Thomma BP, BioEssays 36:335-345, 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Goodwin SB, Cohen BA, Fry WE, Proc Natl Acad Sci USA 91:11591-11595, 1994; Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10:e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, et al. PLoS Pathog 8:e1002940, 2012). However, the dynamics of genome evolution within these clonal lineages have not been determined. The objective of this study was to use a comparative genomics and transcriptomics approach to determine the molecular mechanisms that underpin phenotypic variation within a clonal lineage of P. infestans.
Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by comparing strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Delgado RA, Monteros-Altamirano AR, Li Y, Visser RGF, van der Lee TAJ, Vosman B, Plant Pathol 62:1081-1088, 2013; Forbes GA, Escobar XC, Ayala CC, Revelo J, Ordonez ME, Fry BA, Doucett K, Fry WE, Phytopathology 87:375-380, 1997; Oyarzun PJ, Pozo A, Ordonez ME, Doucett K, Forbes GA, Phytopathology 88:265-271, 1998). We detected numerous examples of structural variation, nucleotide polymorphisms and loss of heterozygosity within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor.
Our findings highlight the molecular changes underpinning the exceptional genetic and phenotypic plasticity associated with host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen. We observed that the asexual P. infestans lineage EC-1 can exhibit phenotypic plasticity in the absence of apparent genetic mutations resulting in virulence on a potato carrying the Rpi-vnt1.1 gene. Such variant alleles may be epialleles that arose through epigenetic changes in the underlying genes.
无性谱系的真菌和卵菌病原体引起的暴发仍然是作物、野生动物和自然生态系统的持续威胁（Fisher MC、Henk DA、Briggs CJ、Brownstein JS、Madoff LC、McCra SL、Gurr SJ、Nature 484:186-194, 2012；Kupferschmidt K、Science 337:636-638, 2012）。然而，无性真核微生物的基因组进化和表型可塑性的机制仍知之甚少（Seidl MF、Thomma BP、BioEssays 36:335-345, 2014）。自 19 世纪爱尔兰饥荒以来，卵菌 Phytophthora infestans 已在马铃薯和番茄作物上引发了反复爆发，这些爆发主要是由流行无性谱系的相继兴起和迁移引起的（Goodwin SB、Cohen BA、Fry WE、Proc Natl Acad Sci USA 91:11591-11595, 1994；Yoshida K、Burbano HA、Krause J、Thines M、Weigel D、Kamoun S、PLoS Pathog 10:e1004028, 2014；Yoshida K、Schuenemann VJ、Cano LM、Pais M、Mishra B、Sharma R、Lanz C、Martin FN、Kamoun S、Krause J、et al. eLife 2:e00731, 2013；Cooke DEL、Cano LM、Raffaele S、Bain RA、Cooke LR、Etherington GJ、Deahl KL、Farrer RA、Gilroy EM、Goss EM、et al. PLoS Pathog 8:e1002940, 2012）。然而，这些克隆谱系内的基因组进化动态尚未确定。本研究的目的是利用比较基因组学和转录组学方法，确定无性谱系内表型变异的分子机制。
在这里，我们通过比较属于自 20 世纪 90 年代以来在安第斯地区流行的南美 EC-1 克隆的菌株，揭示了无性谱系内基因组和基因表达变异的模式（Yoshida K、Burbano HA、Krause J、Thines M、Weigel D、Kamoun S、PLoS Pathog 10:e1004028, 2014；Yoshida K、Schuenemann VJ、Cano LM、Pais M、Mishra B、Sharma R、Lanz C、Martin FN、Kamoun S、Krause J、et al. eLife 2:e00731, 2013；Delgado RA、Monteros-Altamirano AR、Li Y、Visser RGF、van der Lee TAJ、Vosman B、Plant Pathol 62:1081-1088, 2013；Forbes GA、Escobar XC、Ayala CC、Revelo J、Ordonez ME、Fry BA、Doucett K、Fry WE、Phytopathology 87:375-380, 1997；Oyarzun PJ、Pozo A、Ordonez ME、Doucett K、Forbes GA、Phytopathology 88:265-271, 1998）。我们在 EC-1 克隆中检测到大量结构变异、核苷酸多态性和杂合性丧失的例子。值得注意的是，尽管没有序列多态性，但在两个 EC-1 分离株中的一个中，有 17 个基因没有表达。其中，一个效应基因的沉默与马铃薯免疫受体赋予的抗病性的逃避有关。
我们的研究结果强调了与宿主适应相关的无性真核植物病原体大流行克隆谱系的遗传和表型可塑性的分子变化。我们发现，无性 P. infestans 谱系 EC-1 在没有明显遗传突变导致携带 Rpi-vnt1.1 基因的马铃薯致病的情况下，可能表现出表型可塑性。这种变体等位基因可能是通过潜在基因的表观遗传变化产生的表观等位基因。
