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Gibberellin Promotes Shoot Branching in the Perennial Woody Plant Jatropha curcas.

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.

SUBMITTER: Ni J

PROVIDER: S-EPMC4523387 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Project description:Shoot branching from axillary buds (AXBs) is regulated by a network of inhibitory and promotive forces, which includes hormones. In perennials, the dwarfed stature of the embryonic shoot inside AXBs is indicative of gibberellin (GA) deficiency, suggesting that AXB activation and outgrowth require GA. Nonetheless, the role of GA in branching has remained obscure. We here carried out comprehensive GA transcript and metabolite analyses in hybrid aspen, a perennial branching model. The results indicate that GA has an inhibitory as well as promotive role in branching. The latter is executed in two phases. While the expression level of GA2ox is high in quiescent AXBs, decapitation rapidly downregulated it, implying increased GA signaling. In the second phase, GA3ox2-mediated de novo GA-biosynthesis is initiated between 12 and 24 h, prior to AXB elongation. Metabolite analyzes showed that GA1/4 levels were typically high in proliferating apices and low in the developmentally inactive, quiescent AXBs, whereas the reverse was true for GA3/6. To investigate if AXBs are differently affected by GA3, GA4, and GR24, an analog of the branch-inhibitor hormone strigolactone, they were fed into AXBs of single-node cuttings. GA3 and GA4 had similar effects on GA and SL pathway genes, but crucially GA3 induced AXB abscission whereas GA4 promoted outgrowth. Both GA3 and GA4 strongly upregulated GA2ox genes, which deactivate GA1/4 but not GA3/6. Thus, the observed production of GA3/6 in quiescent AXBs targets GA1/4 for GA2ox-mediated deactivation. AXB quiescence can therefore be maintained by GA3/6, in combination with strigolactone. Our discovery of the distinct tasks of GA3 and GA4 in AXB activation might explain why the role of GA in branching has been difficult to decipher. Together, the results support a novel paradigm in which GA3/6 maintains high levels of GA2ox expression and low levels of GA4 in quiescent AXBs, whereas activation and outgrowth require increased GA1/4 signaling through the rapid reduction of GA deactivation and subsequent GA biosynthesis.

Project description:BACKGROUND:In higher plants, inflorescence architecture is an important agronomic trait directly determining seed yield. However, little information is available on the regulatory mechanism of inflorescence development in perennial woody plants. Based on two inflorescence branching mutants, we investigated the transcriptome differences in inflorescence buds between two mutants and wild-type (WT) plants by RNA-Seq to identify the genes and regulatory networks controlling inflorescence architecture in Jatropha curcas L., a perennial woody plant belonging to Euphorbiaceae. RESULTS:Two inflorescence branching mutants were identified in germplasm collection of Jatropha. The duo xiao hua (dxh) mutant has a seven-order branch inflorescence, and the gynoecy (g) mutant has a three-order branch inflorescence, while WT Jatropha has predominantly four-order branch inflorescence, occasionally the three- or five-order branch inflorescences in fields. Using weighted gene correlation network analysis (WGCNA), we identified several hub genes involved in the cytokinin metabolic pathway from modules highly associated with inflorescence phenotypes. Among them, Jatropha ADENOSINE KINASE 2 (JcADK2), ADENINE PHOSPHORIBOSYL TRANSFERASE 1 (JcAPT1), CYTOKININ OXIDASE 3 (JcCKX3), ISOPENTENYLTRANSFERASE 5 (JcIPT5), LONELY GUY 3 (JcLOG3) and JcLOG5 may participate in cytokinin metabolic pathway in Jatropha. Consistently, exogenous application of cytokinin (6-benzyladenine, 6-BA) on inflorescence buds induced high-branch inflorescence phenotype in both low-branch inflorescence mutant (g) and WT plants. These results suggested that cytokinin is an important regulator in controlling inflorescence branching in Jatropha. In addition, comparative transcriptome analysis showed that Arabidopsis homologous genes Jatropha AGAMOUS-LIKE 6 (JcAGL6), JcAGL24, FRUITFUL (JcFUL), LEAFY (JcLFY), SEPALLATAs (JcSEPs), TERMINAL FLOWER 1 (JcTFL1), and WUSCHEL-RELATED HOMEOBOX 3 (JcWOX3), were differentially expressed in inflorescence buds between dxh and g mutants and WT plants, indicating that they may participate in inflorescence development in Jatropha. The expression of JcTFL1 was downregulated, while the expression of JcLFY and JcAP1 were upregulated in inflorescences in low-branch g mutant. CONCLUSIONS:Cytokinin is an important regulator in controlling inflorescence branching in Jatropha. The regulation of inflorescence architecture by the genes involved in floral development, including TFL1, LFY and AP1, may be conservative in Jatropha and Arabidopsis. Our results provide helpful information for elucidating the regulatory mechanism of inflorescence architecture in Jatropha.

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Gibberellin Promotes Shoot Branching in the Perennial Woody Plant Jatropha curcas.

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