Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis

Cyclanilide (CYC), a plant growth regulator, is a potent shoot branching agent in apple. However, its mechanism remains unclear. The current study revealed that CYC treatment resulted in massive reprogramming of the axillary bud transcriptome, implicating several hormones in the response. We observe...

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Main Authors: Juanjuan Ma, Lingling Xie, Qian Zhao, Yiting Sun, Dong Zhang
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/2/581
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author Juanjuan Ma
Lingling Xie
Qian Zhao
Yiting Sun
Dong Zhang
author_facet Juanjuan Ma
Lingling Xie
Qian Zhao
Yiting Sun
Dong Zhang
author_sort Juanjuan Ma
collection DOAJ
description Cyclanilide (CYC), a plant growth regulator, is a potent shoot branching agent in apple. However, its mechanism remains unclear. The current study revealed that CYC treatment resulted in massive reprogramming of the axillary bud transcriptome, implicating several hormones in the response. We observed a marked increase (approximately 2-fold) in the level of zeatin riboside and a significant decrease (approximately 2-fold) in the level of abscisic acid (ABA). Zeatin metabolism gene cytokinin (CTK) oxidase 1 (<i>CKX 1</i>) was down-regulated at 168 h after CYC treatment compared with the control. Weighted gene co-expression network analysis of differentially expressed genes demonstrated the turquoise module clusters exhibited the highest positive correlation with zeatin riboside (r = 0.92) and the highest negative correlation with ABA (r = −0.8). A total of 37 genes were significantly enriched in the plant hormone signal transduction pathway in the turquoise module. Among them, the expressions of CTK receptor genes <i>WOODEN LEG</i> and the CTK type-A response regulators genes <i>ARR3</i> and <i>ARR9</i> were up-regulated. ABA signal response genes protein phosphatase 2C genes <i>ABI2</i> and <i>ABI5</i> were down-regulated in lateral buds after CYC treatment at 168 h. In addition, exogenous application of 6-benzylaminopurine (6-BA, a synthetic type of CTK) and CYC enhanced the inducing effect of CYC, whereas exogenous application of lovastatin (a synthetic type of inhibitor of CTK biosynthesis) or ABA and CYC weakened the promoting effect of CYC. These results collectively revealed that the stimulation of bud growth by CYC might involve CTK biosynthesis and signalling, including genes <i>CKX1</i> and <i>ARR3/9</i>, which provided a direction for further study of the branching promoting mechanism of CYC.
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spelling doaj.art-80e8f3c67ed440548e03b5ebc692f3302023-11-23T14:00:44ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-01-0123258110.3390/ijms23020581Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome AnalysisJuanjuan Ma0Lingling Xie1Qian Zhao2Yiting Sun3Dong Zhang4College of Horticulture, Yangling Subsidiary Center Project of the National Apple Improvement Center, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Horticulture, Yangling Subsidiary Center Project of the National Apple Improvement Center, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Horticulture, Yangling Subsidiary Center Project of the National Apple Improvement Center, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Horticulture, Yangling Subsidiary Center Project of the National Apple Improvement Center, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Horticulture, Yangling Subsidiary Center Project of the National Apple Improvement Center, Northwest A&F University, Yangling, Xianyang 712100, ChinaCyclanilide (CYC), a plant growth regulator, is a potent shoot branching agent in apple. However, its mechanism remains unclear. The current study revealed that CYC treatment resulted in massive reprogramming of the axillary bud transcriptome, implicating several hormones in the response. We observed a marked increase (approximately 2-fold) in the level of zeatin riboside and a significant decrease (approximately 2-fold) in the level of abscisic acid (ABA). Zeatin metabolism gene cytokinin (CTK) oxidase 1 (<i>CKX 1</i>) was down-regulated at 168 h after CYC treatment compared with the control. Weighted gene co-expression network analysis of differentially expressed genes demonstrated the turquoise module clusters exhibited the highest positive correlation with zeatin riboside (r = 0.92) and the highest negative correlation with ABA (r = −0.8). A total of 37 genes were significantly enriched in the plant hormone signal transduction pathway in the turquoise module. Among them, the expressions of CTK receptor genes <i>WOODEN LEG</i> and the CTK type-A response regulators genes <i>ARR3</i> and <i>ARR9</i> were up-regulated. ABA signal response genes protein phosphatase 2C genes <i>ABI2</i> and <i>ABI5</i> were down-regulated in lateral buds after CYC treatment at 168 h. In addition, exogenous application of 6-benzylaminopurine (6-BA, a synthetic type of CTK) and CYC enhanced the inducing effect of CYC, whereas exogenous application of lovastatin (a synthetic type of inhibitor of CTK biosynthesis) or ABA and CYC weakened the promoting effect of CYC. These results collectively revealed that the stimulation of bud growth by CYC might involve CTK biosynthesis and signalling, including genes <i>CKX1</i> and <i>ARR3/9</i>, which provided a direction for further study of the branching promoting mechanism of CYC.https://www.mdpi.com/1422-0067/23/2/581cyclanilideapplebranchingtranscriptomecytokinin
spellingShingle Juanjuan Ma
Lingling Xie
Qian Zhao
Yiting Sun
Dong Zhang
Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
International Journal of Molecular Sciences
cyclanilide
apple
branching
transcriptome
cytokinin
title Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
title_full Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
title_fullStr Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
title_full_unstemmed Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
title_short Cyclanilide Induces Lateral Bud Outgrowth by Modulating Cytokinin Biosynthesis and Signalling Pathways in Apple Identified via Transcriptome Analysis
title_sort cyclanilide induces lateral bud outgrowth by modulating cytokinin biosynthesis and signalling pathways in apple identified via transcriptome analysis
topic cyclanilide
apple
branching
transcriptome
cytokinin
url https://www.mdpi.com/1422-0067/23/2/581
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