Cause and Effectors: Whole-Genome Comparisons Reveal Shared but Rapidly Evolving Effector Sets among Host-Specific Plant-Castrating Fungi
Cause and Effectors: Whole-Genome Comparisons Reveal Shared but Rapidly Evolving Effector Sets among Host-Specific Plant-Castrating Fungi
复制标题
DOI：
10.1128/mbio.02391-19
复制
发表时间：
2019-11-01
期刊：
影响因子：
6.4
通讯作者：
Perlin, Michael H.
中科院分区：
文献类型：
--
作者：
Beckerson, William C.;Rodriguez de la Vega, Ricardo C.;Perlin, Michael H.
植物病原体利用一系列分泌的效应物成功地感染和操纵它们的宿主。然而，目前尚不清楚导致寄主专化的分泌体的变化是否主要涉及效应器基因的获得/丢失或其序列的改变。为了验证这些假说，我们比较了三种寄主特异的去势花药黑粉菌(Microbotryum)的分泌组，其中两种是姊妹种。为了解决可能涉及共同进化和局部适应的种内进化，我们比较了来自不同种群的菌株的分泌体。我们通过实验验证了信号肽的一个子集。分泌组从321到445个预测的分泌蛋白(SP)，包括一些物种特有的蛋白(42到75)，以及有限的拷贝数变化，即很少的基因家族的扩大或减少。52%至68%的SP与任何Pfam结构域都不匹配，小分泌蛋白的这一比例达到80%，表明进化速度很快。与背景基因相比，我们确实发现SPS在物种和菌株之间的分化程度更高，在正选择下更常见，并在植物中高表达；重复诱导点突变(RIPs)在效应器多样化中没有作用，因为SPS不比背景基因更接近转座元件，也不受RIP影响更大。因此，我们的研究确定了保守的核心蛋白，这些蛋白可能是所有微孢子菌病原生命周期所必需的，也可能是物种特有的或在正向选择下进化的蛋白；这些蛋白可能参与了寄主专化和/或共同进化。然而，在与寄主密切相关的病原菌中，大多数变化涉及的是序列的快速变化，而不是基因的获得/丢失。重要的是，植物病原菌使用分子武器成功地感染宿主，分泌大量的各种蛋白质和酶。不同的植物物种经常被寄主特有的病原体寄生；然而，目前尚不清楚这种寄主专门化的分子基础是涉及特定物种的武器还是同一武器的不同变种。因此，我们比较了寄生在不同寄主植物上的三种植物去势病原菌的分泌蛋白编码基因，它们通过替换花粉在植物花药中产生孢子。我们验证了我们对某些基因分泌信号的预测，并检查了我们预测的分泌蛋白在植物感染期间经常高表达。虽然我们发现很少有物种特异性的分泌蛋白，但大量编码分泌蛋白的基因显示出快速进化和自然选择的迹象。因此，我们的研究发现，密切相关的宿主特异性病原体之间的大多数变化涉及共享分子武器的快速适应性变化，而不是新武器的创新。
Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi (Microbotryum), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed in planta; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all Microbotryum species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses.IMPORTANCE Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons.