Department of Biological Sciences, Cunningham Hall, Kent State University, Kent, OH 44240, USA.
Gene. 2011 Jun 15;479(1-2):29-36. doi: 10.1016/j.gene.2011.02.009. Epub 2011 Feb 25.
Glycosyl hydrolase family 28 (GH28) is a set of structurally related enzymes that hydrolyze glycosidic bonds in pectin, and are important extracellular enzymes for both pathogenic and saprotrophic fungi. Yet, very little is understood about the evolutionary forces driving the diversification of GH28s in fungal genomes. We reconstructed the evolutionary history of family GH28 in fungi by examining the distribution of GH28 copy number across the phylogeny of fungi, and by reconstructing the phylogeny of GH28 genes. We also examined the relationship between lineage-specific GH28 expansions and fungal ecological strategy, testing the hypothesis that GH28 evolution in fungi is driven by ecological strategy (pathogenic vs. non-pathogenic) and pathogenic niche (necrotrophic vs. biotrophic). Our results showed that GH28 phylogeny of Ascomycota and Basidiomycota sequences was structured by specific biochemical function, with endo-polygalacturonases and endo-rhamnogalacturonases forming distinct, apparently ancient clades, while exo-polygalacturonases are more widely distributed. In contrast, Mucoromycotina and Stramenopile sequences formed taxonomically-distinct clades. Large, lineage-specific variation in GH28 copy number indicates that the evolution of this gene family is consistent with the birth-and-death model of gene family evolution, where diversity of GH28 loci within genomes was generated through multiple rounds of gene duplication followed by functional diversification and loss of some gene family members. Although GH28 copy number was correlated with genome size, our findings suggest that ecological strategy also plays an important role in determining the GH28 repertoire of fungi. Both necrotrophic and biotrophic fungi have larger genomes than non-pathogens, yet only necrotrophs possess more GH28 enzymes than non-pathogens. Hence, lineage-specific GH28 expansion is the result of both variation in genome size across fungal species and diversifying selection within the necrotrophic plant pathogen ecological niche. GH28 evolution among necrotrophs has likely been driven by a co-evolutionary arms race with plants, whereas the need to avoid plant immune responses has resulted in purifying selection within biotrophic fungi.
糖苷水解酶家族 28（GH28）是一组结构相关的酶，能够水解果胶中的糖苷键，是病原真菌和腐生真菌的重要细胞外酶。然而，对于驱动真菌基因组中 GH28 多样化的进化力量，我们知之甚少。我们通过检查 GH28 拷贝数在真菌系统发育中的分布，以及重建 GH28 基因的系统发育，来重建真菌中 GH28 家族的进化历史。我们还研究了谱系特异性 GH28 扩张与真菌生态策略之间的关系，检验了 GH28 在真菌中的进化是由生态策略（病原与非病原）和病原小生境（坏死与生物）驱动的假设。研究结果表明，子囊菌和担子菌的 GH28 系统发育结构由特定的生化功能决定，内聚半乳糖醛酸酶和内切鼠李半乳糖醛酸酶形成不同的、显然古老的分支，而外切半乳糖醛酸酶的分布则更为广泛。相比之下，毛霉门和不等鞭毛门的序列形成了分类学上不同的分支。GH28 拷贝数的大量、谱系特异性变化表明，该基因家族的进化与基因家族进化的“诞生与死亡”模型一致，即基因组中 GH28 基因座的多样性是通过多轮基因复制产生的，随后是功能多样化和一些基因家族成员的丢失。尽管 GH28 拷贝数与基因组大小相关，但我们的研究结果表明，生态策略在决定真菌的 GH28 库方面也起着重要作用。坏死型和生物型真菌的基因组都比非病原真菌大，但只有坏死型真菌比非病原真菌拥有更多的 GH28 酶。因此，谱系特异性 GH28 扩张是真菌物种间基因组大小变化和坏死型植物病原菌生态小生境中多样化选择的结果。坏死型真菌中 GH28 的进化很可能是与植物的共同进化军备竞赛的结果，而避免植物免疫反应导致了生物型真菌中的纯化选择。
