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（1,3,7-三甲基黄嘌呤，1,3,7-trimethixanthine）是一种典型的嘌呤生物碱，在超过80种植物中合成。其生物学功能被认为是增强植物的防御能力：一方面作为有毒物质直接作用于生物入侵者（化感作用，allelopathy），另一方面作为防御系统的激活剂间接发挥调控作用（防御启动，priming）。咖啡因可通过主根（primary root）主动分泌至根际（rhizosphere）环境，进而可能影响周边微生物群落的结构。咖啡树根际的真菌群落中富集有特定类群，其中包括木霉菌科（Trichoderma）——一类通过缠绕并破坏病原菌菌丝（hyphae）来侵染并杀死植物病原菌（phytopathogens）的重寄生真菌（mycoparasite）。本研究针对8株丝状真菌（filamentous fungi）展开咖啡因响应分析，其中包括4株重寄生木霉菌以及4株作为寄主的植物病原菌。研究结果显示，咖啡因对真菌生长发育的化感作用存在显著差异：对病原菌的抑制效果强于对木霉菌的作用。当暴露于咖啡因环境时，作为寄主的病原菌会立即停止生长，而捕食者木霉菌则可继续增殖，这表明活跃的重寄生作用已被触发。咖啡因可将重寄生作用效率提升至1.7倍。由此可见，咖啡因对植物病原菌的拮抗作用遵循双重机制：其一为直接抑制病原菌的生长发育，其二为协助其天敌发挥作用。上述研究结果表明，咖啡因通过强化病原菌天敌的功能，在植物与病原菌的军备竞赛中扮演了强力武器的角色；据此我们提出“咖啡因促生（caffeine fostering）”假说，将其作为咖啡因的第三类生物学功能。