Article ; Online: Jasmonoyl-L-isoleucine coordinates metabolic networks required for anthesis and floral attractant emission in wild tobacco (Nicotiana attenuata).
2014 Volume 26, Issue 10, Page(s) 3964–3983
Abstract: ... maturation. The binding of jasmonoyl-L-isoleucine (JA-Ile) to the F-box of CORONATINE INSENSITIVE1 (COI1) is ...
| 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. |
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| MeSH term(s) | Abscisic Acid/metabolism ; Abscisic Acid/pharmacology ; Acetates/metabolism ; Acetates/pharmacology ; Acetone/analogs & derivatives ; Acetone/metabolism ; Amino Acids/metabolism ; Amino Acids/pharmacology ; Animals ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Cyclopentanes/metabolism ; Cyclopentanes/pharmacology ; Esterases/genetics ; Esterases/metabolism ; Flowers/drug effects ; Flowers/genetics ; Flowers/metabolism ; Gene Expression Profiling ; Gene Expression Regulation, Plant/drug effects ; Indenes/metabolism ; Indenes/pharmacology ; Isoleucine/analogs & derivatives ; Isoleucine/metabolism ; Isoleucine/pharmacology ; Manduca/physiology ; Metabolic Networks and Pathways ; Methyltransferases/genetics ; Methyltransferases/metabolism ; Models, Biological ; Oligonucleotide Array Sequence Analysis ; Oxylipins/metabolism ; Oxylipins/pharmacology ; Plant Growth Regulators/metabolism ; Plant Growth Regulators/pharmacology ; Plant Nectar/metabolism ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Plants, Genetically Modified ; Pollination ; RNA Interference ; Reverse Transcriptase Polymerase Chain Reaction ; Nicotiana/drug effects ; Nicotiana/genetics ; Nicotiana/metabolism |
| Chemical Substances | Acetates ; Amino Acids ; Arabidopsis Proteins ; Cyclopentanes ; Indenes ; Oxylipins ; Plant Growth Regulators ; Plant Nectar ; Plant Proteins ; benzyl acetone ; jasmonoyl-isoleucine ; Isoleucine (04Y7590D77) ; Acetone (1364PS73AF) ; coronatine (62251-96-1) ; jasmonic acid (6RI5N05OWW) ; Abscisic Acid (72S9A8J5GW) ; methyl jasmonate (900N171A0F) ; Methyltransferases (EC 2.1.1.-) ; jasmonic acid carboxyl methyltransferase (EC 2.1.1.-) ; Esterases (EC 3.1.-) |
| Language | English |
| Publishing date | 2014-10-17 |
| Publishing country | England |
| Document type | Journal Article ; Research Support, Non-U.S. Gov't |
| ZDB-ID | 623171-8 |
| ISSN | 1532-298X ; 1040-4651 |
| ISSN (online) | 1532-298X |
| ISSN | 1040-4651 |
| DOI | 10.1105/tpc.114.128165 |
| Database | MEDical Literature Analysis and Retrieval System OnLINE |
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