Sugarcane smut caused by Sporisorium scitamineum seriously impairs sugarcane production and quality. Sexual mating/filamentation is a critical step of S. scitamineum pathogenesis, yet the regulatory mechanisms are not fully understood. In this study, we identified the SsAGA, SsODC, and SsSAMDC genes, which are involved in polyamine biosynthesis in S. scitamineum. Deletion of SsODC led to complete loss of filamentous growth after sexual mating, and deletion of SsAGA or SsSAMDC caused reduced filamentation. Double deletion of SsODC and SsSAMDC resulted in auxotrophy for putrescine (PUT) and spermidine (SPD) when grown on minimal medium (MM), indicating that these two genes encode enzymes that are critical for PUT and SPD biosynthesis. We further showed that low PUT concentrations promoted S. scitamineum filamentation, while high PUT concentrations suppressed filamentation. Disrupted fungal polyamine biosynthesis also resulted in a loss of pathogenicity and reduced fungal biomass within infected plants at the early infection stage. SPD formed a gradient from the diseased part to nonsymptom parts of the cane stem, suggesting that SPD is probably favourable for fungal virulence. Mutants of the cAMP–PKA (SsGPA3–SsUAC1–SsADR1) signalling pathway displayed up-regulation of the SsODC gene and elevated intracellular levels of PUT. SsODC directly interacted with SsGPA3, and sporidia of the ss1uac1ΔodcΔ mutant displayed abundant pseudohyphae. Furthermore, we found that elevated PUT levels caused accumulation of intracellular reactive oxygen species (ROS), probably by suppressing transcription of ROS-scavenging enzymes, while SPD played the opposite role. Overall, our work proves that polyamines play important roles in the pathogenic development of sugarcane smut fungus, probably by collaboratively regulating intracellular redox homeostasis with the cAMP–PKA signalling pathway.

中文翻译：

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细胞内多胺在性交配/丝状形成过程中通过 cAMP-PKA 信号调节氧化还原稳态以及 Scitamineum 孢子虫的致病性

由甘蔗黑穗病引起的甘蔗黑穗病严重影响甘蔗产量和质量。有性交配/丝状形成是S. scitamineum发病机制的关键步骤，但其调节机制尚不完全清楚。在这项研究中，我们鉴定了SsAGA、SsODC和SsSAMDC基因，这些基因参与S. scitamineum的多胺生物合成。SsODC的缺失导致性交配后丝状生长完全丧失，SsAGA或SsSAMDC的缺失导致丝状形成减少。当在基本培养基（MM）上生长时， SsODC和SsSAMDC的双重缺失导致腐胺（PUT）和亚精胺（SPD）营养缺陷，表明这两个基因编码对PUT和SPD生物合成至关重要的酶。我们进一步表明，低 PUT 浓度促进Scitamineum丝状形成，而高 PUT 浓度抑制丝状形成。真菌多胺生物合成的破坏还导致感染早期受感染植物内的致病性丧失和真菌生物量减少。SPD 形成从甘蔗茎的患病部分到无症状部分的梯度，表明 SPD 可能有利于真菌毒力。cAMP-PKA (SsGPA3-SsUAC1-SsADR1) 信号通路突变体显示SsODC基因上调和 PUT 细胞内水平升高。SsODC 直接与 SsGPA3 相互作用，ss1uac1 Δ odc Δ 突变体的孢子虫表现出丰富的假菌丝。此外，我们发现 PUT 水平升高可能通过抑制 ROS 清除酶的转录而导致细胞内活性氧 (ROS) 的积累，而 SPD 则发挥相反的作用。总的来说，我们的工作证明多胺在甘蔗黑穗病真菌的致病发展中发挥着重要作用，可能是通过与 cAMP-PKA 信号通路协同调节细胞内氧化还原稳态来实现的。