Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations.
The plant hormone jasmonic acid (JA) plays a pivotal role in plant-insect interactions. Herbivore attack usually elicits dramatic increases in JA concentrations, which in turn activate the accumulation of metabolites that function as defenses against herbivores. Although almost all enzymes involved in the biosynthesis pathway of JA have been identified and characterized, the mechanism by which plants regulate JA biosynthesis remains unclear. Calcium-dependent protein kinases (CDPKs) are plant-specific proteins that sense changes in [Ca(2+)] to activate downstream responses. We created transgenic Nicotiana attenuata plants, in which two CDPKs, NaCDPK4 and NaCDPK5, were simultaneously silenced (IRcdpk4/5 plants). IRcdpk4/5 plants were stunted and aborted most of their flower primordia. Importantly, after wounding or simulated herbivory, IRcdpk4/5 plants accumulated exceptionally high JA levels. When NaCDPK4 and NaCDPK5 were silenced individually, neither stunted growth nor high JA levels were observed, suggesting that NaCDPK4 and NaCDPK5 have redundant roles. Attack from Manduca sexta larvae on IRcdpk4/5 plants induced high levels of defense metabolites that slowed M. sexta growth. We found that NaCDPK4 and NaCDPK5 affect plant resistance against insects in a JA- and JA-signaling-dependent manner. Furthermore, IRcdpk4/5 plants showed overactivation of salicylic-acid-induced protein kinase, a mitogen-activated protein kinase involved in various stress responses, and genetic analysis indicated that the increased salicylic-acid-induced protein kinase activity in IRcdpk4/5 plants was a consequence of the exceptionally high JA levels and was dependent on CORONATINE INSENSITIVE1. This work reveals the critical roles of CDPKs in modulating JA homeostasis and highlights the complex duet between JA and mitogen-activated protein kinase signaling.
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
Da-Hai
DH
Yang
Christian
C
Hettenhausen
Ian T
IT
Baldwin
Jianqiang
J
Wu
D000818:Animals; D003517:Cyclopentanes / Q000378:metabolism*; D035264:Flowers / Q000201:enzymology; D055785:Gene Knockdown Techniques; D020868:Gene Silencing; D060434:Herbivory / Q000502:physiology*; D018402:Manduca / Q000502:physiology; D020929:Mitogen-Activated Protein Kinase Kinases / Q000378:metabolism; D020928:Mitogen-Activated Protein Kinases / Q000378:metabolism; D008954:Models, Biological; D008969:Molecular Sequence Data; D054883:Oxylipins / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D018547:Plant Stems / Q000201:enzymology; D011494:Protein Kinases / Q000235:genetics* / Q000378:metabolism; D015398:Signal Transduction; D014026:Nicotiana / Q000201:enzymology* / Q000254:growth & development / Q000469:parasitology / Q000502:physiology; D015854:Up-Regulation; D017871:Calcium-Calmodulin-Dependent Protein Kinases
D003517:Cyclopentanes; D020929:Mitogen-Activated Protein Kinase Kinases; D020928:Mitogen-Activated Protein Kinases; D054883:Oxylipins; D010940:Plant Proteins; D011494:Protein Kinases; D017871:Calcium-Calmodulin-Dependent Protein Kinases; C011006:jasmonic acid; C113423:WIPK protein, Nicotiana tabacum; C404401:salicylic acid-induced protein kinase kinase