A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) reduces growth and increases secondary metabolite biosynthesis in herbivore-attacked plants

• Published in: The New phytologist 2015-10, Vol.208 (2), p.519-530
• Main Authors: Ferrieri, Abigail P., Arce, Carla C. M., Machado, Ricardo A. R., Meza‐Canales, Ivan D., Lima, Eraldo, Baldwin, Ian T., Erb, Matthias
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Animals; Attenuation; beta-Fructofuranosidase - antagonists & inhibitors; Biosynthesis; Carbohydrate metabolism; Carbohydrate Metabolism - drug effects; Carbohydrates; Catabolism; Cell Wall - drug effects; Cell Wall - metabolism; cell wall invertase; Cell walls; Cloning, Molecular; Cyclopentanes - pharmacology; Depletion; DNA, Complementary - genetics; Gene expression; Gene Silencing - drug effects; Herbivores; Herbivory; Herbivory - drug effects; Inhibitors; Invertase; invertase inhibitor; jasmonate (JA); Jasmonic acid; Larva - drug effects; Larva - physiology; Manduca - drug effects; Manduca - physiology; Manduca sexta; Metabolism; Metabolites; Molecular Sequence Data; Nicotiana - cytology; Nicotiana - drug effects; Nicotiana - growth & development; Nicotiana - parasitology; Nicotiana attenuata; Oxylipins - pharmacology; plant defense; Plant growth; Plant Growth Regulators - pharmacology; Plant Proteins - chemistry; Plant Proteins - metabolism; RNA-mediated interference; Secondary Metabolism - drug effects; Source-sink relationships; Up-Regulation - drug effects
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.13475

Plant invertases are sucrolytic enzymes that are essential for the regulation of carbohydrate metabolism and source–sink relationships. While their activity has been well documented during abiotic and biotic stresses, the role of proteinaceous invertase inhibitors in regulating these changes is unknown. Here, we identify a putative Nicotiana attenuata cell wall invertase inhibitor (NaCWII) which is strongly up-regulated in a jasmonate (JA)-dependent manner following simulated attack by the specialist herbivore Manduca sexta. To understand the role of NaCWII in planta, we silenced its expression by RNA interference and measured changes in primary and secondary metabolism and plant growth following simulated herbivory. NaCWII-silenced plants displayed a stronger depletion of carbohydrates and a reduced capacity to increase secondary metabolite pools relative to their empty vector control counterparts. This coincided with the attenuation of herbivore-induced CWI inhibition and growth suppression characteristic of wild-type plants. Together our findings suggest that NaCWII may act as a regulatory switch located downstream of JA accumulation which fine-tunes the plant's balance between growth and defense metabolism under herbivore attack. Although carbohydrates are not typically viewed as key factors in plant growth and defense, our study shows that interfering with their catabolism strongly influences plant responses to herbivory.