Sebacina vermifera promotes the growth and fitness of Nicotiana attenuata by inhibiting ethylene signaling.
Sebacina vermifera, a growth-promoting endophytic fungus, significantly increases Nicotiana attenuata's growth but impairs both its herbivore resistance and its accumulation of the costly, jasmonic acid (JA)-regulated defense protein, trypsin proteinase inhibitor (TPI). To determine if the fungi's growth-promoting effects can be attributed to lower TPI-related defense costs, we inoculated transformed N. attenuata plants silenced in their ability to synthesize JA, JA-isoleucine, and TPI by antisense (lipoxygenase 3 [as-lox3] and Thr deaminase [as-td]) and inverted repeat (ir-tpi) expression, and found that inoculation promoted plant growth as in untransformed wild-type plants. Moreover, herbivore-elicited increases in JA and JA-isoleucine concentrations did not differ between inoculated and uninoculated wild-type plants. However, inoculation significantly reduced the morphological effect of 1-aminocyclopropane-1-carboxylic acid on wild-type seedlings in a triple response assay, suggesting that ethylene signaling was impaired. Furthermore, S. vermifera failed to promote the growth of N. attenuata plants transformed to silence ethylene production (1-aminocyclopropane-1-carboxylic acid oxidase [ir-aco]). Inoculating wild-type plants with S. vermifera decreased the ethylene burst elicited by applying Manduca sexta oral secretions to mechanical wounds. Accordingly, oral secretion-elicited transcript levels of the ethylene synthesis genes NaACS3, NaACO1, and NaACO3 in inoculated plants were significantly lower compared to these levels in uninoculated wild-type plants. Inoculation accelerated germination in wild-type seeds; however, uninoculated wild-type seeds germinated as rapidly as inoculated seeds in the presence of the ethylene scrubber KMnO(4). In contrast, neither inoculation nor KMnO(4) exposure influenced the germination of ir-aco seeds. We conclude that S. vermifera increases plant growth by impairing ethylene production independently of JA signaling and TPI production.
Barazani
Oz
O
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Beutenberg Campus, 07745 Jena, Germany.
von Dahl
Caroline C
CC
Baldwin
Ian T
IT
D000818:Animals; D001487:Basidiomycota / Q000502:physiology*; D019755:Carbon-Carbon Lyases / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism; D005030:Ethylenes / Q000037:antagonists & inhibitors / Q000378:metabolism*; D020868:Gene Silencing; D018525:Germination / Q000502:physiology; D007814:Larva / Q000502:physiology; D018402:Manduca / Q000502:physiology; D009055:Mouth / Q000378:metabolism; D054883:Oxylipins; D036226:Seedlings / Q000254:growth & development; D012639:Seeds / Q000382:microbiology; D015398:Signal Transduction / Q000502:physiology; D013559:Symbiosis / Q000502:physiology*; D014026:Nicotiana / Q000382:microbiology* / Q000502:physiology; D014158:Transcription, Genetic; D014361:Trypsin Inhibitors / Q000378:metabolism
D003517:Cyclopentanes; D005030:Ethylenes; D054883:Oxylipins; D014361:Trypsin Inhibitors; C011006:jasmonic acid; C036216:ethylene; C033634:1-aminocyclopropane-1-carboxylate deaminase; D019755:Carbon-Carbon Lyases