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. 2015 Aug;56(8):1655-66.
doi: 10.1093/pcp/pcv089. Epub 2015 Jun 15.

Gibberellin Promotes Shoot Branching in the Perennial Woody Plant Jatropha curcas

Jun Ni  1 , Congcong Gao  2 , Mao-Sheng Chen  2 , Bang-Zhen Pan  2 , Kaiqin Ye  3 , Zeng-Fu Xu  4
Affiliations

Gibberellin Promotes Shoot Branching in the Perennial Woody Plant Jatropha curcas

Jun Ni et al. Plant Cell Physiol. 2015 Aug.

Abstract

Strigolactone (SL), auxin and cytokinin (CK) interact to regulate shoot branching. CK has long been considered to be the only key phytohormone to promote lateral bud outgrowth. Here we report that gibberellin also acts as a positive regulator in the control of shoot branching in the woody plant Jatropha curcas. We show that gibberellin and CK synergistically promote lateral bud outgrowth, and that both hormones influence the expression of putative branching regulators, J. curcas BRANCHED1 and BRANCHED2, which are key transcription factors maintaining bud dormancy. Moreover, treatment with paclobutrazol, an inhibitor of de novo gibberellin biosynthesis, significantly reduced the promotion of bud outgrowth by CK, suggesting that gibberellin is required for CK-mediated axillary bud outgrowth. In addition, SL, a plant hormone involved in the repression of shoot branching, acted antagonistically to both gibberellin and CK in the control of lateral bud outgrowth. Consistent with this, the expression of JcMAX2, a J. curcas homolog of Arabidopsis MORE AXILLARY GROWTH 2 encoding an F-box protein in the SL signaling pathway, was repressed by gibberellin and CK treatment. We also provide physiological evidence that gibberellin also induces shoot branching in many other trees, such as papaya, indicating that a more complicated regulatory network occurs in the control of shoot branching in some perennial woody plants.

Keywords: Axillary bud; Bud outgrowth; Cytokinin; Gibberellin; Shoot branching; Strigolactone.

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Figures

Fig. 1
Fig. 1
GA3 and BA promote shoot branching in J. curcas. (A) Shoot branching stimulated by GA3 or BA treatment in the young stems of 2-year-old J. curcas trees. (B) The number of induced branches was counted 4 weeks after GA3 (500 mg l–1) or BA (500 mg l–1) treatment (n = 30). (C) The number of stimulated axillary buds was counted 1 and 2 weeks after the application of various concentrations of GA3 to the top region of the branch (∼20 cm; n = 28–45). (D) Representative lateral bud stimulated by GA3 treatment in 2-year-old J. curcas trees. (E) Axillary bud length at nodes 1–3 of 4-week-old J. curcas seedlings measured 2 weeks after GA3 or BA treatment (n = 12–14). (F) Buds at nodes 1–3 of 5-week-old J. curcas seedlings showed different responsiveness to GA3 or BA (500 μM) treatment (n > 20). (G) Lateral bud on an old stem of a 3-year-old J. curcas tree, stimulated by GA3 or BA (500 μM) treatment. Values are means ± SE for (B), (C), (E) and (F). Student’s t-test was used to determine significant differences between the indicated groups in (B) or between the treated and control groups in (C), (E) and (F). Significance levels: *P < 0.05; **P < 0.01. Red arrows indicate the stimulated axillary buds.
Fig. 2
Fig. 2
GA3 and BA synergistically stimulate bud outgrowth in 3-week-old seedlings of J. curcas. (A) Photographs showing representative outgrowth of the buds at node 1 at 1, 2 and 3 weeks after treatment (WAT 1, 2 and 3), respectively. Red arrows indicate the stimulated axillary buds. Scale bars = 1 cm. (B) Outgrowth of the buds at node 1 (n = 24). (C) Outgrowth of the buds at node 2 at 2 weeks after treatment (n > 20). Treatments were conducted at node 1 with GA3 (500 μM), BA (500 μM) or GA3 + BA. Values are means SE. Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: **P < 0.01.
Fig. 3
Fig. 3
Co-application of GA3 and BA at low concentrations effectively promoted lateral bud outgrowth in 3-week-old seedlings of J. curcas. (A) Outgrowth of the buds at node 1 stimulated by GA3 + BA treatment. Photos were taken at 1 and 2 weeks after treatment (WAT 1 and 2). Red arrows indicate the stimulated axillary buds. Scale bars = 1 cm. (B) The length of the buds at nodes 1 and 2 was measured at 1 or 2 weeks after treatment with 10–200 μM GA3 + BA. (C) The length of the buds at nodes 1 was measured at 1 week after treatment with 0.1–5 μM GA3 + BA. Data are means ±SE (n = 20). Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: *P < 0.05; **P < 0.01.
Fig. 4
Fig. 4
Paclobutrazol (PAC) inhibits promotion of bud outgrowth by BA. (A, B) PAC decreased the number of stimulated axillary buds and the outgrowth of buds in 4-week-old seedlings subjected to shoot treatment with BA (n > 15). The concentrations of PAC and BA used in single or combined treatments in (A) and (B) are 200 and 500 μM respectively. (C) Promotion of outgrowth of buds at node 1 by bud treatment with BA (200 μM) was inhibited by co-application of PAC (200 μM). Red arrows indicate the stimulated axillary buds. Scale bars = 1 cm. (D) Bud outgrowth of buds at node 1 by bud treatment with BA (200 μM) in conjunction with different concentrations of PAC (n = 20). All data and photos in (A–D) were taken at 1 week after treatment. Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: **P < 0.01.
Fig. 5
Fig. 5
CK is required for promotion of bud outgrowth by gibberellin in the root-excised 3-week-old seedlings of J. curcas. (A) The length of buds at node 1 at 1 week after treatment with GA3 (200 μM) or GA3 (200 μM) + BA (20 μM) (n = 20). (B) Addition of various concentrations of BA in the liquid culture promoted the outgrowth of buds at node 1 at 1 week after GA3 treatment (n = 20). (C) Photographs of outgrowth of lateral buds at node 1 promoted by treatment with GA3 (200 μM) in conjunction with or without various concentrations of BA in the liquid culture. Red arrows indicated the buds that became dormant after 2 weeks growth. Scale bars = 1 cm. Root excision was conducted 2 d before hormone treatment. Values are means ± SE. Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: **P < 0.01; NS, not significant.
Fig. 6
Fig. 6
GA3, but not BA, induces lateral bud outgrowth on the newly developed shoots of 2-year-old J. curcas trees. (A) Secondary lateral buds (indicated by red arrows) were induced by treatment of shoots with GA3 (500 μM), but not BA (500 μM). (B) The number of lateral buds induced by treatment of shoot apex with GA3 or BA (n = 31–33). Values are means ± SE. Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: **P < 0.01; NS indicates no significant differences. (C) GA3 treatment at the shoot apex led to an obvious outgrowth of lateral buds (indicated by red arrows) on the newly developed shoots, while BA treatment did not. Scale bars = 1 cm.
Fig. 7
Fig. 7
Effects of GA3, BA and decapitation on the expression of JcBRC1 and JcBRC2 at node 1 of 3-week-old J. curcas seedlings. (A) GA3 or BA (500 μM) treatment decreased the expression of JcBRC1 and JcBRC2 (n = 3). (B) Decapitation decreased the expression of JcBRC1 and JcBRC2 (n = 3). Decapitation was conducted on the 3-week-old seedlings by removing the shoot tip (approximately 1 cm). Samples for qPCR analysis were collected at 24 h after treatment. Values are means ± SE. Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: *P < 0.05; **P < 0.01.
Fig. 8
Fig. 8
Strigolactones antagonistically regulates lateral bud outgrowth in J. curcas seedlings treated with GA3 and BA. (A–C) Bud outgrowth at node 1 of 3-week-old seedlings 1 week after GA3, BA, GR24, BA + GR24 or GA3 + GR24 treatments. Scale bars = 1 cm (n = 20). (D) GA3 and BA decreased the expression of JcMAX2 at node 1 (n = 3). (E) Decapitation decreased the expression of JcMAX2 at 24 h after treatment (n = 3). The concentration of BA, GA3 and GR24 used in (A), (B) and (D) was 200, 200 and 50 μM, respectively. Values are means ± SE for (B–E). Student’s t-test was used to determine significant differences between the indicated groups in (B) or between the treated and control groups in (C–E). Significance levels: *P < 0.05; **P < 0.01.
Fig. 9
Fig. 9
GA3 promotes lateral bud outgrowth in papaya. (A) One-year-old papaya tree. (B) Six-week-old papaya seedlings. (C) Bud length at node 2 of 6-week-old papaya seedlings was measured 3 weeks after GA3 or BA treatment (n = 32–34). The axillary buds of papaya were directly treated with GA3 (500 μM) or BA (500 μM) solution. Values are means ± SE for (C). Student’s t-test was used to determine significant differences between the treated and control groups. Significance levels: **P < 0.01.
Fig. 10
Fig. 10
GA3 promotes the lateral bud outgrowth in other tree plants. The top approximately 20 cm of the selected branches was sprayed with 500 μM GA3 or the control solutions every other day twice. The red arrows indicate the stimulated lateral buds. Scale bars = 1 cm.
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