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First published online February 20, 2009
doi: 10.1242/10.1242/dev.030585

Development 136, 1039-1048 (2009)
Published by The Company of Biologists 2009
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Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis

Yuki Yoshida1,2, Ryosuke Sano3, Takuji Wada3, Junji Takabayashi2 and Kiyotaka Okada1,4,*

1 Department of Botany, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.
2 Center for Ecological Research, Kyoto University, Otsu 520-2113, Japan.
3 Plant Science Center, RIKEN, Yokohama 230-0045, Japan.
4 National Institute for Basic Biology, Okazaki 444-8585, Japan.


Figure 1
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  		Fig. 1. Wound-induced trichome formation in Arabidopsis is dependent on jasmonates (JAs). (A,B) 16-DAG (days after germination) wild-type Col-0 grown under standard conditions (A) or wounded on 8 DAG (B). (C,D) Scanning electron micrograph of the adaxial epidermis of developing leaves from 10-DAG Col-0; untreated (C) or methyl jasmonate (MeJA)-treated on 6 DAG (D). Note the differences in branch numbers as well as in the texture of cell wall surface. (E) Quantification of trichome numbers in the fifth true leaves with or without wounding (mean±s.e. of at least 12 plants). (F-H) The trichome morphology of aos and coi1-1 is indistinguishable from that of Col-0. Scale bars: 1 mm in A,B,F-H; 100 µm in C,D.

 

Figure 2
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  		Fig. 2. Allelic series of GL1 shows a distinct trichome-induction phenotype. (A) The domain structure of three paralogous R2R3-Myb proteins, GL1, MYB23 and WER, as well as of three gl1 mutants from Arabidopsis. Colored boxes represent conserved domains. The bHLH-interaction motif overlaps the R3 Myb domain. The C-terminal transcriptional activator domain has a cluster of acidic residues (red asterisks). (B) Quantification of trichome number in gl1 and myb23 mutants with or without wounding (mean±s.e. of at least 12 plants). Zero indicates no trichomes produced. (C,D) 16-DAG gl1-2 grown under standard conditions (C) or wounded on 8 DAG (D). Scale bars: 1 mm.

 

Figure 3
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  		Fig. 3. MYB23 is expressed and functions late in trichome induction. (A,B) Expression analysis of GL2 and CPC in gl1-2 mutants. MeJA treatment of gl1-2 triggered de novo formation of trichomes marked with GL2::GUS (A) and CPC::GFP (B) expression. gl1-2 myb23-1 lacks GL2::GUS expression (A). (C) GL1::GUS and MYB23::GUS expression in gl1-2. GL1::GUS is ubiquitously expressed in immature epidermal cells and later confined to developing trichomes, if treated with MeJA. MYB23::GUS is expressed in MeJA-induced trichomes but not in immature epidermal cells. (D-H) Epidermal phenotype of gl1-2 myb23-1. gl1-2 myb23-1 is completely glabrous (D) and remains superficially glabrous after MeJA treatment or wounding (E). However, after MeJA treatment or wounding gl1-2 myb23-1 produces numerous small bulges on the epidermis (F), which resemble arrested trichomes of gl2 (G). Trichomes of gl1-2 myb23-1 are frequently formed in a cluster of two to four cells (H, arrowhead). Scale bars: 100 µm in A,C,F-H; 1 mm in B,D,E.

 

Figure 4
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  		Fig. 4. Phenotypes of Arabidopsis urm9 and urm23 mutants. (A) urm9 single mutant. (B) MeJA-treated urm9 gl1-2 producing a few trichomes (arrowheads). (C) urm23 single mutant. (D) MeJA-treated urm23 gl1-2 with no trichomes. Note that anthocyanin synthesis is normally induced by MeJA in both urm9 and urm23 (B,D, arrows). (E) Dose-response curve of trichome density plotted against the strength of MeJA treatment. (F) Quantification of trichome number in urm9 and urm23 single mutants (mean±s.e. of at least 12 plants). (G,H) Systemic induction of JA-responsive VSP1::GUS expression by wounding. The wounded sites are indicated by arrowheads. Scale bars: 1 mm.

 

Figure 5
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  		Fig. 5. urm9 disrupts the subnuclear localization of GL3. (A,B) The overall expression pattern of GL3::GL3-2xGFP in the young leaf of gl1-2 mutants. Green, GFP; red, chlorophyll autofluorescence to mark the leaf shape. The two leaves (A and B) are at different developmental stages. (C-H) Subcellular localization of GL3::GL3-2xGFP in the adaxial epidermal cells of gl1-2 (C,D), urm9 gl1-2 (E,G,H) or urm9 GL1 (F). Cells shown in C,D,F-H are from leaves that are comparable in size (800 µm to 1 mm), whereas E represents a much younger leaf (400 µm). Initially, a subset of cells exhibits abnormal subnuclear distribution of GL3-2xGFP in urm9 gl1-2 (E, arrowheads). The degree of abnormality of GL3-2xGFP distribution in urm9 gl1-2 varies between cells, with no recognizable pattern (G,H). (I,J) Suppression of the gl3-sst phenotype by urm9. (K,L) Enhancement of the gl3-11 phenotype by urm9. Trichomes are lost around the midvein in urm9 gl3-11 (L). Scale bars: 500 µm in A,B; 10 µm in C-H; 1 mm in I-L.

 

Figure 6
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  		Fig. 6. GL3 is essential for JA-induced trichome formation. (A) Quantification of the trichome numbers in Arabidopsis fifth true leaves with or without MeJA treatment (mean±s.e. of at least 12 plants). Zero indicates no trichomes produced. (B) gl1-2. (C) MeJA-treated gl1-2. Note that the petioles accumulate anthocyanin (arrow). (D) MeJA-treated gl3-11 gl1-2 completely lacking trichome induction. (E) MeJA-treated gl3-11/+ gl1-2 with only a few induced trichomes (arrowheads). (F) gl3-sst/+ partially restored trichome formation in gl1-2 without MeJA treatment. (G) MeJA-treated gl3-sst/+ gl1-2 with dense trichomes. Scale bars: 1 mm.

 

Figure 7
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  		Fig. 7. MeJA-responsive expression of GL3::GL3-2xGFP. Epifluorescence images taken under the same setting to compare the intensity of GFP fusion expression. Shown are representative images from at least 20 plants examined. (A-D) gl1-2 GL3::GL3-2xGFP. (E-H) urm9 gl1-2 GL3::GL3-2xGFP. Plants were either left untreated (A,C,E,G) or treated with MeJA on 6 DAG (B,D,F,H). GFP fluorescence was observed and photographed on 7 DAG (24 hours post-treatment; A,B,E,F) and on 8 DAG (48 hours post-treatment; C,D,G,H). In response to MeJA treatment, both gl1-2 and urm9 gl1-2 induced ubiquitous GL3-2xGFP expression in the adaxial epidermis of young leaves (C,D,G,H). The difference between MeJA-treated and untreated plants was first visible 24 hours post-treatment (A,B,E,F). Scale bars: 1 mm.

 

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