Roy J. Carver Department of Biochemistry, Biophysics & Molecular Biology, Iowa State University, Ames, Iowa, USA.
Department of Veterinary Microbiology and Preventive Medicine, Iowa State University, Ames, Iowa, USA.
mSphere. 2020 Jun 3;5(3):e00292-20. doi: 10.1128/mSphere.00292-20.
Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both symbiotic nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA signaling is a powerful mechanism for microbes to gain an advantage in these interactions. Although orthologous operons encode GA biosynthetic enzymes in both rhizobia and phytopathogens, notable genetic heterogeneity and scattered operon distribution in these lineages, including loss of the gene for the final biosynthetic step in most rhizobia, suggest varied functions for GA in these distinct plant-microbe interactions. Therefore, deciphering GA operon evolutionary history should provide crucial evidence toward understanding the distinct biological roles for bacterial GA production. To further establish the genetic composition of the GA operon, two operon-associated genes that exhibit limited distribution among rhizobia were biochemically characterized, verifying their roles in GA biosynthesis. This enabled employment of a maximum parsimony ancestral gene block reconstruction algorithm to characterize loss, gain, and horizontal gene transfer (HGT) of GA operon genes within alphaproteobacterial rhizobia, which exhibit the most heterogeneity among the bacteria containing this biosynthetic gene cluster. Collectively, this evolutionary analysis reveals a complex history for HGT of the entire GA operon, as well as the individual genes therein, and ultimately provides a basis for linking genetic content to bacterial GA functions in diverse plant-microbe interactions, including insight into the subtleties of the coevolving molecular interactions between rhizobia and their leguminous host plants. While production of phytohormones by plant-associated microbes has long been appreciated, identification of the gibberellin (GA) biosynthetic operon in plant-associated bacteria has revealed surprising genetic heterogeneity. Notably, this heterogeneity seems to be associated with the lifestyle of the microbe; while the GA operon in phytopathogenic bacteria does not seem to vary to any significant degree, thus enabling production of bioactive GA, symbiotic rhizobia exhibit a number of GA operon gene loss and gain events. This suggests that a unique set of selective pressures are exerted on this biosynthetic gene cluster in rhizobia. Through analysis of the evolutionary history of the GA operon in alphaproteobacterial rhizobia, which display substantial diversity in their GA operon structure and gene content, we provide insight into the effect of lifestyle and host interactions on the production of this phytohormone by plant-associated bacteria.
赤霉素（GA）植物激素是维管植物生长和发育过程的普遍调节剂。植物相关细菌产生 GA 的趋同进化，包括共生固氮根瘤菌和植物病原菌，表明微生物操纵 GA 信号是在这些相互作用中获得优势的强大机制。尽管同源操纵子在根瘤菌和植物病原菌中都编码 GA 生物合成酶，但这些谱系中存在显著的遗传异质性和分散的操纵子分布，包括大多数根瘤菌中最后一个生物合成步骤的基因缺失，表明 GA 在这些不同的植物-微生物相互作用中具有不同的功能。因此，破译 GA 操纵子的进化历史应该为理解细菌 GA 产生的不同生物学作用提供关键证据。为了进一步确定 GA 操纵子的遗传组成，对在根瘤菌中分布有限的两个与操纵子相关的基因进行了生化特征分析，验证了它们在 GA 生物合成中的作用。这使得能够使用最大简约祖先基因块重建算法来表征 α 变形菌根瘤菌中 GA 操纵子基因的缺失、获得和水平基因转移（HGT），这些基因在含有该生物合成基因簇的细菌中表现出最大的异质性。总的来说，这种进化分析揭示了整个 GA 操纵子及其内部基因的 HGT 的复杂历史，并最终为将遗传内容与不同植物-微生物相互作用中的细菌 GA 功能联系起来提供了基础，包括深入了解根瘤菌与其豆科宿主植物之间协同进化的分子相互作用的微妙之处。虽然植物相关微生物产生植物激素早已被人们所认识，但在植物相关细菌中鉴定出赤霉素（GA）生物合成操纵子揭示了令人惊讶的遗传异质性。值得注意的是，这种异质性似乎与微生物的生活方式有关；虽然植物病原菌中的 GA 操纵子似乎没有任何显著的变化，从而能够产生生物活性的 GA，但共生根瘤菌表现出许多 GA 操纵子基因的缺失和获得事件。这表明，一套独特的选择压力施加在根瘤菌的这个生物合成基因簇上。通过分析 α 变形菌根瘤菌中 GA 操纵子的进化历史，我们了解到其 GA 操纵子结构和基因组成的多样性，为我们提供了关于生活方式和宿主相互作用对植物相关细菌产生这种植物激素的影响的见解。
