title: Jasmonoyl-L-isoleucine coordinates metabolic networks required for anthesis and floral attractant emission in wild tobacco (Nicotiana attenuata).
abstract: Jasmonic acid and its derivatives (jasmonates [JAs]) play central roles in floral development and maturation. The binding of jasmonoyl-L-isoleucine (JA-Ile) to the F-box of CORONATINE INSENSITIVE1 (COI1) is required for many JA-dependent physiological responses, but its role in anthesis and pollinator attraction traits remains largely unexplored. Here, we used the wild tobacco Nicotiana attenuata, which develops sympetalous flowers with complex pollination biology, to examine the coordinating function of JA homeostasis in the distinct metabolic processes that underlie flower maturation, opening, and advertisement to pollinators. From combined transcriptomic, targeted metabolic, and allometric analyses of transgenic N. attenuata plants for which signaling deficiencies were complemented with methyl jasmonate, JA-Ile, and its functional homolog, coronatine (COR), we demonstrate that (1) JA-Ile/COR-based signaling regulates corolla limb opening and a JA-negative feedback loop; (2) production of floral volatiles (night emissions of benzylacetone) and nectar requires JA-Ile/COR perception through COI1; and (3) limb expansion involves JA-Ile-induced changes in limb fresh mass and carbohydrate metabolism. These findings demonstrate a master regulatory function of the JA-Ile/COI1 duet for the main function of a sympetalous corolla, that of advertising for and rewarding pollinator services. Flower opening, by contrast, requires JA-Ile signaling-dependent changes in primary metabolism, which are not compromised in the COI1-silenced RNA interference line used in this study.
authors.affiliation: Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, 07745 Jena, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Stitz
authors.affiliation: Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, 07745 Jena, Germany.
authors.forename: Markus
authors.initials: M
authors.lastname: Hartl
authors.affiliation: Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, 07745 Jena, Germany.
authors.forename: Ian T
authors.initials: IT
authors.lastname: Baldwin
authors.affiliation: Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, 07745 Jena, Germany Centre for Organismal Studies, University of Heidelberg, 69120 Heidelberg, Germany emmanuel.gaquerel@cos.uni-heidelberg.de.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Gaquerel
mesh_terms: D000040:Abscisic Acid / Q000378:metabolism / Q000494:pharmacology; D000085:Acetates / Q000378:metabolism / Q000494:pharmacology; D000096:Acetone / Q000031:analogs & derivatives / Q000378:metabolism; D000596:Amino Acids / Q000378:metabolism / Q000494:pharmacology; D000818:Animals; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism* / Q000494:pharmacology; D004950:Esterases / Q000235:genetics / Q000378:metabolism; D035264:Flowers / Q000187:drug effects / Q000235:genetics / Q000378:metabolism*; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D007192:Indenes / Q000378:metabolism / Q000494:pharmacology; D007532:Isoleucine / Q000031:analogs & derivatives* / Q000378:metabolism / Q000494:pharmacology; D018402:Manduca / Q000502:physiology; D053858:Metabolic Networks and Pathways; D008780:Methyltransferases / Q000235:genetics / Q000378:metabolism; D008954:Models, Biological; D020411:Oligonucleotide Array Sequence Analysis; D054883:Oxylipins / Q000378:metabolism / Q000494:pharmacology; D010937:Plant Growth Regulators / Q000378:metabolism / Q000494:pharmacology; D057048:Plant Nectar / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D054817:Pollination; D034622:RNA Interference; D020133:Reverse Transcriptase Polymerase Chain Reaction; D014026:Nicotiana / Q000187:drug effects / Q000235:genetics / Q000378:metabolism*
chemical_list: D000085:Acetates; D000596:Amino Acids; D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D007192:Indenes; D054883:Oxylipins; D010937:Plant Growth Regulators; D057048:Plant Nectar; D010940:Plant Proteins; C531285:benzyl acetone; C532883:jasmonoyl-isoleucine; D007532:Isoleucine; D000096:Acetone; C058487:coronatine; C011006:jasmonic acid; D000040:Abscisic Acid; C072239:methyl jasmonate; D008780:Methyltransferases; C425043:jasmonic acid carboxyl methyltransferase; D004950:Esterases