Caffeine fostering of mycoparasitic fungi against phytopathogens

Caffeine (1,3,7-trimethixanthine) is a typical purine alkaloid produced in more than 80 plant species. Its biological role is considered to strengthen plant's defense capabilities, directly as a toxicant to biotic attackers (allelopathy) and indirectly as an activator of defense system (priming). Caffeine is actively secreted into rhizosphere through primary root, and possibly affects the structure of microbe community nearby. The fungal community in coffee plant rhizosphere is enriched with particular species, including Trichoderma family, a mycoparasite that attacks and kills phytopathogens by coiling and destroying their hyphae. In the present study, the caffeine response of 8 filamentous fungi, 4 mycoparasitic Trichoderma, and 4 prey phytopathogens, was examined. Results showed that allelopathic effect of caffeine on fungal growth and development was differential, being stronger on pathogens than on Trichoderma species. Upon confronting, the prey immediately ceased the growth, whereas the predator continued to grow, indicating active mycoparasitism to have occurred. Caffeine enhanced mycoparasitism up to 1.7-fold. Caffeine thus functions in a double-track manner against fungal pathogens: first by direct suppression of growth and development, and second by assisting their natural enemy. These observations suggest that caffeine is a powerful weapon in the arms race between plants and pathogens by fostering enemy's enemy, and we propose the idea of "caffeine fostering" as the third role of caffeine.

咖啡因（Caffeine，1,3,7-三甲基黄嘌呤）是一类典型的嘌呤生物碱，在超过80种植物中均有合成。其生物学功能被认为是增强植物的防御能力：既可作为有毒物质直接作用于生物入侵者，发挥化感作用（allelopathy）；也可作为防御系统激活剂，间接启动植物的防御通路。咖啡因可通过主根主动分泌至根际（rhizosphere）环境，进而可能改变周边微生物群落的结构。咖啡树根际的真菌群落富集了特定类群，包括木霉菌属（Trichoderma）——一类重寄生真菌（mycoparasite），可通过缠绕并破坏病原菌菌丝来侵染并杀死植物病原菌（phytopathogens）。本研究针对8株丝状真菌开展了咖啡因响应实验，其中包含4株重寄生木霉菌与4株靶标植物病原菌。实验结果显示，咖啡因对真菌生长发育的化感效应存在显著差异：对病原菌的抑制作用强于木霉菌。当二者接触时，靶标病原菌会立即停止生长，而木霉菌（捕食者）则可继续生长，表明重寄生作用已被激活。咖啡因可将重寄生作用效率提升至1.7倍。由此可见，咖啡因通过双重机制对抗植物病原菌：其一为直接抑制病原菌的生长发育，其二为协助其天然天敌发挥作用。上述研究结果表明，咖啡因可通过“培育天敌的天敌”参与植物与病原菌间的军备竞赛（arms race），我们据此提出“咖啡因培育（caffeine fostering）”作为咖啡因第三类生物学功能的新概念。