State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources/Guangdong Province Key Laboratory of Microbial Signals and Disease Control/Integrative Microbiology Research Centre, South China Agricultural Universitygrid.20561.30, Guangzhou, China.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China.
Microbiol Spectr. 2022 Aug 31;10(4):e0057022. doi: 10.1128/spectrum.00570-22. Epub 2022 Jul 6.
Sugarcane smut caused by the basidiomycetous fungus Sporisorium scitamineum leads to severe economic losses globally. Sexual mating/filamentation of S. scitamineum is critical for its pathogenicity, as only the dikaryotic hyphae formed after sexual mating are capable of invading the host cane. Our comparative transcriptome analysis showed that the mitogen-activated protein kinase (MAPK) pathway and the AGC kinase Agc1 (orthologous to yeast Rim15), both governing mating/filamentation, were induced by elevated tryptophol level, supporting a positive regulation of mating/filamentation by tryptophol. However, the biosynthesis pathway of tryptophol remains unknown in . Here, we identified an aminotransferase orthologous to the established tryptophan aminotransferase Tam1/Aro8, catalyzing the first step of tryptophan-dependent indole-3-acetic acid (IAA) production as well as that of the Ehrlich pathway for tryptophol production. We designated this aminotransferase as SsAro8 and found that it was essential for mating/filamentation. Comparative metabolomics analysis revealed that SsAro8 was involved in tryptophan metabolism, likely for producing important intermediate products, including tryptophol. Exogenous addition of tryptophan or tryptophol could differentially restore mating/filamentation in the Δ mutant, indicating that in addition to tryptophol, other product(s) of tryptophan catabolism may also be involved in mating/filamentation regulation. could also produce IAA, partially dependent on SsAro8 function. Surprisingly, photodestruction of IAA produced the compound(s) able to suppress growth/differentiation. Lastly, we found that SsAro8 was required for proper biofilm formation, oxidative stress tolerance, and full pathogenicity in . Overall, our study establishes the aminotransferase SsAro8 as an essential regulator of pathogenic differentiation, as well as fungus-host interaction, and therefore of great potential as a molecular target for sugarcane smut disease control. Sugarcane smut caused by the basidiomycete fungus leads to massive economic losses in sugarcane plantation globally. Dikaryotic hyphae formation (filamentous growth) and biofilm formation are two important aspects in pathogenesis, yet the molecular regulation of these two processes was not as extensively investigated as that in the model pathogenic fungi, e.g., Candida albicans, Ustilago maydis, or Cryptococcus neoformans. In this study, a tryptophan aminotransferase ortholog was identified in , designated SsAro8. Functional characterization showed that SsAro8 positively regulates both filamentous growth and biofilm formation, respectively, via tryptophol-dependent and -independent manners. Furthermore, SsAro8 is required for full pathogenicity and, thus, is a promising molecular target for designing anti-smut strategy.
由担子菌真菌盾壳霉引起的甘蔗黑粉病在全球范围内造成严重的经济损失。盾壳霉的有性交配/菌丝形成对于其致病性至关重要，因为只有有性交配后形成的双核菌丝才能侵入宿主甘蔗。我们的比较转录组分析表明，调节交配/菌丝形成的丝裂原激活蛋白激酶（MAPK）途径和 AGC 激酶 Agc1（与酵母 Rim15 同源）被色氨酸水平升高诱导，这支持了色氨酸对交配/菌丝形成的正向调节。然而，盾壳霉中色氨酸的生物合成途径仍然未知。在这里，我们鉴定了一个与已建立的色氨酸氨基转移酶 Tam1/Aro8 同源的氨基转移酶，它催化色氨酸依赖性吲哚-3-乙酸（IAA）产生的第一步以及 Ehrlich 途径中色醇产生的第一步。我们将这个 氨基转移酶命名为 SsAro8，并发现它对交配/菌丝形成是必需的。比较代谢组学分析表明，SsAro8 参与色氨酸代谢，可能产生重要的中间产物，包括色醇。外源性添加色氨酸或色醇可以在 Δ突变体中差异恢复交配/菌丝形成，表明除了色醇之外，色氨酸分解代谢的其他产物也可能参与交配/菌丝形成的调节。 也可以产生 IAA，部分依赖于 SsAro8 的功能。令人惊讶的是，IAA 的光破坏产生了能够抑制 生长/分化的化合物。最后，我们发现 SsAro8 是 正确生物膜形成、氧化应激耐受和完全致病性所必需的。总的来说，我们的研究确立了氨基转移酶 SsAro8 作为 致病分化以及真菌-宿主相互作用的重要调节剂，因此作为甘蔗黑粉病防治的分子靶标具有很大的潜力。
