Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses

Abstract

BackgroundJasmonates are well known plant signaling components required for stress responses and development. A prominent feature of jasmonate biosynthesis or signaling mutants is the loss of fertility. In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development. Its senescence phenotype suggests a function of jasmonates in regulation of processes known to be mediated by ethylene. To test the hypothesis that ethylene involved in tomato stamen development is regulated by jasmonates, a temporal profiling of hormone content, transcriptome and metabolome of tomato stamens was performed using wild type and jai1-1.ResultsWild type stamens showed a transient increase of jasmonates that is absent in jai1-1. Comparative transcriptome analyses revealed a diminished expression of genes involved in pollen nutrition at early developmental stages of jai1-1 stamens, but an enhanced expression of ethylene-related genes at late developmental stages. This finding coincides with an early increase of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in jai1-1 and a premature pollen release from stamens, a phenotype similarly visible in an ethylene overproducing mutant. Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.ConclusionsOur data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0135-3) contains supplementary material, which is available to authorized users.

Overexpression of a tomato miR171 target gene SlGRAS24 impacts multiple agronomical traits via regulating gibberellin and auxin homeostasis

“…In the nonexhaustive list of genes differentially regulated between SlGRAS24 ‐OE and WT flowers (Table ), 15 are related to pollen development, 13 are associated with hormones and 19 are transcription factors. Most phytohormones play crucial roles in the regulation of pollen development either directly (Song et al ., ) or indirectly (Dobritzsch et al ., ; Ji et al ., ). Our results demonstrated altered expression of genes related to all hormones except GA (Table ).…”

Auxin-Induced Modulation of ETTIN Activity Orchestrates Gene Expression in Arabidopsis

“…Genes connected with ethylene and JA were also enriched in the set of direct ETT targets. Since ett mutants are severely affected in stamen and pollen morphology (Sessions et al, 1997), and considering the function of ethylene and JA in stamen development and pollination (Dobritzsch et al, 2015), it is plausible that aspects of the ett phenotype are caused by defects in ethylene and JA homeostasis.…”

Fertility of Pedicellate Spikelets in Sorghum is Controlled by a Jasmonic Acid Regulatory Module

“…JA is integral to environmental responsiveness and developmental progression; regulators of JA, JA biosynthetic genes, and JA signaling proteins influence pest/pathogen sensitivity(38, 39), wound response(22, 40, 41), cell expansion(33), and sex determination and floral organ progression (specifically, anther and pistil development)(7, 15–17, 22, 27, 42, 43). Barley, rice, and maize display complex mechanisms of floral development.…”