TY - JOUR
T1 - Transcriptional Reprogramming Deploys a Compartmentalized ‘Timebomb’ in Catharanthus roseus to Fend Off Chewing Herbivores
AU - Liu, Yongliang
AU - Shi, Jizhe
AU - Patra, Barunava
AU - Singh, Sanjay Kumar
AU - Wu, Xia
AU - Lyu, Ruiqing
AU - Liu, Xiaoyu
AU - Li, Yongqing
AU - Wang, Ying
AU - Zhou, Xuguo
AU - Pattanaik, Sitakanta
AU - Yuan, Ling
N1 - Publisher Copyright:
© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.
PY - 2024
Y1 - 2024
N2 - 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.
AB - 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.
KW - Catharanthus roseus
KW - cold tolerance
KW - herbivory resistance
KW - insect–plant interaction
KW - terpenoid indole alkaloid
KW - timebomb
KW - transcriptional reprogramming
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U2 - 10.1111/pce.15324
DO - 10.1111/pce.15324
M3 - Article
C2 - 39718032
AN - SCOPUS:85212834104
SN - 0140-7791
JO - Plant, Cell and Environment
JF - Plant, Cell and Environment
ER -