Liu Yongliang, Shi Jizhe, Patra Barunava, Singh Sanjay Kumar, Wu Xia, Lyu Ruiqing, Liu Xiaoyu, Li Yongqing, Wang Ying, Zhou Xuguo, Pattanaik Sitakanta, Yuan Ling
Department of Plant and Soil Sciences and Kentucky Tobacco Research and Development Center, University of Kentucky, Lexington, Kentucky, USA.
Department of Entomology, University of Kentucky, Martin-Gatton College of Agriculture, Food and Environment, Lexington, Kentucky, USA.
Plant Cell Environ. 2025 May;48(5):3236-3256. doi: 10.1111/pce.15324. Epub 2024 Dec 24.
The evolutionary arms race between plants and insects has led to key adaptive innovations that drive diversification. Alkaloids are well-documented anti-herbivory compounds in plant chemical defences, but how these specialized metabolites are allocated to cope with both biotic and abiotic stresses concomitantly is largely unknown. To examine how plants prioritize their metabolic resources responding to herbivory and cold, we integrated dietary toxicity bioassay in insects with co-expression analysis, hierarchical clustering, promoter assay, and protein-protein interaction in plants. Catharanthus roseus, a medicinal plant known for its insecticidal property against chewing herbivores, produces two terpenoid indole alkaloid monomers, vindoline and catharanthine. Individually, they exhibited negligible toxicity against Manduca sexta, a chewing herbivore; their condensed product, anhydrovinblastine; however, was highly toxic. Such a unique insecticidal mode of action demonstrates that terpenoid indole alkaloid 'timebomb' can only be activated when the two spatially isolated monomeric precursors are dimerized by herbivory. Without initial selection pressure and apparent fitness costs, this adaptive chemical defence against herbivory is innovative and sustainable. The biosynthesis of insecticidal terpenoid indole alkaloids is induced by herbivory but suppressed by cold. Here, we identified a transcription factor, herbivore-induced vindoline-gene Expression (HIVE), that coordinates the production of terpenoid indole alkaloids in response to herbivory and cold stress. The HIVE-mediated transcriptional reprogramming allows this herbaceous perennial to allocate its metabolic resources for chemical defence at a normal temperature when herbivory pressure is high, but switches to cold tolerance under a cooler temperature when insect infestation is secondary.
植物与昆虫之间的进化军备竞赛催生了推动多样化的关键适应性创新。生物碱是植物化学防御中记载充分的抗食草化合物，但这些特殊代谢产物如何分配以同时应对生物和非生物胁迫在很大程度上尚不清楚。为了研究植物如何优先分配其代谢资源以应对食草和寒冷，我们将昆虫的饮食毒性生物测定与植物中的共表达分析、层次聚类、启动子测定和蛋白质-蛋白质相互作用相结合。长春花是一种以对咀嚼式食草动物具有杀虫特性而闻名的药用植物，它产生两种萜类吲哚生物碱单体，文朵灵和长春质碱。单独来看，它们对咀嚼式食草动物烟草天蛾的毒性可忽略不计；然而，它们的缩合产物脱水长春碱却具有剧毒。这种独特的杀虫作用方式表明，萜类吲哚生物碱“定时炸弹”只有在两个空间隔离的单体前体因食草作用而二聚化时才会被激活。在没有初始选择压力和明显的适应性成本的情况下，这种针对食草的适应性化学防御具有创新性和可持续性。杀虫萜类吲哚生物碱的生物合成受食草诱导，但受寒冷抑制。在这里，我们鉴定出一种转录因子，即食草动物诱导的文朵灵基因表达（HIVE），它能协调萜类吲哚生物碱在应对食草和寒冷胁迫时的产生。HIVE介导的转录重编程使这种多年生草本植物在食草压力高的常温下将其代谢资源分配用于化学防御，但在温度较低且昆虫侵扰为次要因素时切换为耐寒性。
