High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems

Abstract

SUMMARYHormones play pivotal roles in regulating plant development, growth, and stress responses, and cross-talk among different hormones fine-tunes various aspects of plant physiology. Jasmonic acid (JA) is important for plant defense against herbivores and necrotic fungi and also regulates flower development; in addition, Arabidopsis mutants over-producing JA usually have stunted stems and wound-induced jasmonates suppress Arabidopsis growth, suggesting that JA is also involved in stem elongation. Gibberellins (GAs) promote stem and leaf growth and modulate seed germination, flowering time, and the development of flowers, fruits, and seeds. However, little is known about the interaction between the JA and GA pathways. Two calcium-dependent protein kinases, CDPK4 and CDPK5, are important suppressors of JA accumulation in a wild tobacco species, Nicotiana attenuata. The stems of N. attenuata silenced in CDPK4 and CDPK5 (irCDPK4/5 plants) had dramatically increased levels of JA and exhibited stunted elongation and had very high contents of secondary metabolites. Genetic analysis indicated that the high JA levels in irCDPK4/5 stems accounted for the suppressed stem elongation and the accumulation of secondary metabolites. Supplementation of GA 3 to irCDPK4/5 plants largely restored normal stem growth to wild-type levels. Measures of GA levels indicated that over-accumulation of JA in irCDPK4/5 stems inhibited the biosynthesis of GAs. Finally, we show that JA antagonizes GA biosynthesis by strongly inhibiting the transcript accumulation of GA20ox and possibly GA13ox, the key genes in GA production, demonstrating that high JA levels antagonize GA biosynthesis in stems.

Repression of lateral organ boundary genes by PENNYWISE and POUND-FOOLISH is essential for meristem maintenance and flowering in Arabidopsis thaliana1

“…Inhibitory effects of MeJA on flowering are also reported in Pharbitis nil (Maciejewska and Kopceiwicz, 2002;Maciejewska et al, 2004), Chenopodium rubrum (Albrechtová and Ullmann, 1994), and einkorn wheat (Triticum monococcum; Diallo et al, 2014). JA antagonism of growth or flowering has been linked to repression of GA biosynthesis (Magome et al, 2004;Heinrich et al, 2013), stabilization of DELLAs (Yang et al, 2012), and/or induction of AP2/ERF factors (Magome et al, 2008;Sun et al, 2008;Kang et al, 2011;Licausi et al, 2013). These data are consistent with JA contributing to bop1-6D and pny pnf developmental defects.…”

“…These data support the findings by Canet et al (2012), which identified BOP1/2 as essential for MeJA induced in priming for resistance to Pseudomonas syringae pv tomato DC3000. Plants exposed to high levels of jasmonate are stunted in growth of roots, leaves, and stems (Ellis et al, 2002;Cipollini, 2005;Bonaventure et al, 2007;Hyun et al, 2008;Zhang and Turner, 2008;Heinrich et al, 2013). Arabidopsis plants treated with jasmonate are also late flowering with short internodes and loss of apical dominance, giving an appearance similar to bop1-6D or pny pnf/+ mutants.…”

“…Its targets include SPL genes, which are also directly activated by SOC1 and FD Porri et al, 2012). How these various pathways are integrated with stress signals is an area of active study (Yang et al, 2012;Heinrich et al, 2013;Hou et al, 2013;Diallo et al, 2014;Stief et al, 2014).…”

The Reductase Activity of the Arabidopsis Caleosin RESPONSIVE TO DESSICATION20 Mediates Gibberellin-Dependent Flowering Time, Abscisic Acid Sensitivity, and Tolerance to Oxidative Stress

“…When RD20 is overexpressed, 13-HPOT, which is a precursor of JA, might be channeled away from the JA biosynthetic pathway to be converted into 13-HOT, thus leading to reduced JA levels. JA has been reported to antagonize the GA signaling pathway and GA biosynthesis by inhibiting the accumulation of Ga20ox and Ga3ox transcripts (Heinrich et al, 2013). If this occurs in lines overexpressing RD20, reduced JA accumulation could result in early flowering of these lines.…”

The Calcium-Dependent Protein Kinase CPK28 Regulates Development by Inducing Growth Phase-Specific, Spatially Restricted Alterations in Jasmonic Acid Levels Independent of Defense Responses in Arabidopsis

“…An underlying mechanism has been suggested for the direct interaction between respective DELLA and JASMONATE-ZIM DOMAIN (JAZ) repressor proteins (Hou et al, 2010;Wild et al, 2012;Yang et al, 2012b). Interestingly, virus-induced gene silencing (VIGS)-induced cosuppression of Nicotiana attenuata CDPK4 and CDPK5, two close homologs of At-CPK28, resulted in reduced gene expression of GA biosynthetic enzymes and decreased GA phytohormone content, correlating with the observed plant growth reduction on the one hand and elevated JA levels mediating subsequent resistance toward larval feeding on the other hand (Yang et al, 2012a;Heinrich et al, 2013). However, these experiments do not indicate whether developmental phenotypes are directly caused by JA signaling or simply reflect resource reallocation from growth to defense mediated by JA.…”