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. 2008 Mar;146(3):952-64.
doi: 10.1104/pp.107.115691. Epub 2008 Jan 25.

Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory

Hoo Sun Chung  1 , Abraham J K Koo, Xiaoli Gao, Sastry Jayanty, Bryan Thines, A Daniel Jones, Gregg A Howe
Affiliations

Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory

Hoo Sun Chung et al. Plant Physiol. 2008 Mar.

Abstract

Jasmonate (JA) and its amino acid conjugate, jasmonoyl-isoleucine (JA-Ile), play important roles in regulating plant defense responses to insect herbivores. Recent studies indicate that JA-Ile promotes the degradation of JASMONATE ZIM-domain (JAZ) transcriptional repressors through the activity of the E(3) ubiquitin-ligase SCF(COI1). Here, we investigated the regulation and function of JAZ genes during the interaction of Arabidopsis (Arabidopsis thaliana) with the generalist herbivore Spodoptera exigua. Most members of the JAZ gene family were highly expressed in response to S. exigua feeding and mechanical wounding. JAZ transcript levels increased within 5 min of mechanical tissue damage, coincident with a large (approximately 25-fold) rise in JA and JA-Ile levels. Wound-induced expression of JAZ and other CORONATINE-INSENSITIVE1 (COI1)-dependent genes was not impaired in the jar1-1 mutant that is partially deficient in the conversion of JA to JA-Ile. Experiments performed with the protein synthesis inhibitor cycloheximide provided evidence that JAZs, MYC2, and genes encoding several JA biosynthetic enzymes are primary response genes whose expression is derepressed upon COI1-dependent turnover of a labile repressor protein(s). We also show that overexpression of a modified form of JAZ1 (JAZ1Delta3A) that is stable in the presence of JA compromises host resistance to feeding by S. exigua larvae. These findings establish a role for JAZ proteins in the regulation of plant anti-insect defense, and support the hypothesis that JA-Ile and perhaps other JA derivatives activate COI1-dependent wound responses in Arabidopsis. Our results also indicate that the timing of JA-induced transcription in response to wounding is more rapid than previously realized.

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Figures

Figure 1.
Figure 1.
Expression of JAZ genes in response to herbivore feeding and mechanical wounding. A, Five-week-old wild-type plants were challenged with S. exigua larvae. At the indicated times (h) after feeding, damaged local (L) leaves and undamaged systemic (S) leaves were harvested for RNA extraction. A separate set of unchallenged plants was used as a control (C). Five micrograms of total RNA was loaded in each lane and blots were hybridized with the indicated cDNA probes. ACTIN8 (ACT8) was used as a loading control. JAZ4- and JAZ11-probed blots were exposed to autoradiographic film for 16 h, whereas all other blots were exposed for 6 h. The contrast of JAZ4-probed blots was adjusted to facilitate visualization of the JAZ4 signal. B, Five-week-old wild-type plants were wounded three times across the midrib with a hemostat and damaged leaves were collected for RNA extraction at the indicated times (h) after wounding. Ten micrograms of total RNA was loaded in each lane and blots were hybridized to gene-specific probes for each of the 12 JAZ genes, as well as ACT8 as a loading control. JAZ4-, JAZ11-, and ACT8-probed blots were exposed to autoradiographic film for 16 h, whereas all other blots were exposed for 5 h.
Figure 2.
Figure 2.
Effect of the coi1-1 mutation on wound-induced expression of JAZs. Mechanical wound treatments and RNA gel-blot analysis were performed as described in the legend to Figure 1B. Damaged leaves were collected for RNA extraction at the indicated times (min) after wounding. Blots were hybridized to gene-specific probes for each of the indicated JAZ genes, MYC2, and ACT8 as a loading control. All blots were exposed to autoradiographic film for 8 h.
Figure 3.
Figure 3.
Rapid induction of JAZ transcripts and accumulation of JAs in response to mechanical wounding. A, RNA gel-blot analysis of JAZ expression in wounded leaves. Wound treatments and northern-blot analyses were performed as described in the Figure 1B legend. Damaged leaves were collected for RNA extraction at the indicated times (min) after wounding. MYC2- and JAZ-probed blots were exposed to autoradiographic film for 4 and 14 h, respectively. B and C, Time course of JA (B) and JA-Ile (C) accumulation in response to mechanical wounding. Leaf tissue from the same set of plants used for RNA blot analysis (A) was harvested at the indicated time points after wounding for extraction of JAs, as described in “Materials and Methods”. JA and JA-Ile (measured as the total of JA-Ile plus JA-Leu) levels were determined by liquid chromatography-mass spectrometry according to the procedure described in “Materials and Methods.” Each data point represents the mean ±sd of four biological replicates.
Figure 4.
Figure 4.
Wound-induced expression of JA-responsive genes in the jar1-1 mutant. Five-week-old wild-type, coi1-1, and jar1-1 plants were mechanically wounded as described in the legend to Figure 1B. Damaged leaves were collected for RNA extraction at the indicated times (h) after mechanical wounding. Blots were hybridized to probes for MYC2, JAZ5, JAZ7, two JA biosynthesis genes (AOS and OPR3), as well as ACT8 as a loading control. All blots except ACT8 were exposed to autoradiographic film for 6 h. The ACT8 blot was exposed for 16 h.
Figure 5.
Figure 5.
Effect of cycloheximide treatment on JA-responsive genes. A, Twelve-day-old wild-type seedlings grown in liquid medium were treated with either a mock control (0.2% DMSO), 50 μm MeJA (MJ), 50 μm cycloheximide (CHX), or a combination of MeJA and CHX (MJ + CHX) as described in “Materials and Methods”. Whole seedlings were collected for RNA extraction at the indicated times (h) after treatment. Five micrograms of total RNA was loaded in each lane and blots were hybridized to the indicated probes (see text). ACT8 was used as a loading control. LOX3- and LOX4-probed blots were exposed to film for 14 h, whereas all other blots were autoradiographed for 3 h. B, Effect of coi1-1 on CHX-induced expression of JA-responsive genes. CHX treatment and RNA gel-blot analysis were performed as described above. All blots were autoradiographed for 4 h.
Figure 6.
Figure 6.
coi1-1 plants are deficient in wound-induced accumulation of JA. Rosette leaves on 5-week-old wild-type (black circles) and coi1-1 mutant (white circles) plants were mechanically wounded at the distal end with a hemostat. Wounded leaves were harvested for JA extraction at the indicated times (h) after wounding. Unwounded leaf tissue was used as a control for the 0-h time point. Each data point represents the mean ±sd of three samples from independent sets of plants.
Figure 7.
Figure 7.
JAZ1Δ3A plants are compromised in resistance to feeding by S. exigua. A, Newly hatched S. exigua larvae were reared on wild-type (WT in the image) and JAZ1Δ3A transgenic plants. Larval weights were measured 9 and 13 d after the start of the feeding trial. Values indicate the mean ±se. The number of wild-type-reared larvae at the 9- and 13-d time points was 79 and 73, respectively, whereas the number of JAZ1Δ3A-reared larvae was 87 and 111, respectively. B, Representative S. exigua larvae recovered wild-type and JAZ1Δ3A plants at the 13-d time point. C, Expression of various wound-responsive genes in undamaged control (C) and S. exigua-damaged (W) wild-type and JAZ1Δ3A plants. The arrow in C denotes a higher-Mr JAZ1 transcript that presumably is derived from the JAZ1Δ3A-GUS transgene. RNA was extracted from S. exigua-damaged leaves collected at the 13-d time point, or from a set of undamaged plants grown in parallel. Northern-blot analyses were performed as described in the Figure 1 legend.
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