Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.

Polyploid breeding techniques aid in the cultivation of new forestry cultivars, thus expanding the suite of strategies for the improvement of arboreal traits and innovation within the field of forestry. Compared to diploid <i>Robinia pseudoacacia</i> L. (black locust) ‘D26-5①’ (2×), its...

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Main Authors: Yue Wu, Qi Guo, Cui Long, Yousry A. El-Kassaby, Yuhan Sun, Yun Li
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/2/1312
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author Yue Wu
Qi Guo
Cui Long
Yousry A. El-Kassaby
Yuhan Sun
Yun Li
author_facet Yue Wu
Qi Guo
Cui Long
Yousry A. El-Kassaby
Yuhan Sun
Yun Li
author_sort Yue Wu
collection DOAJ
description Polyploid breeding techniques aid in the cultivation of new forestry cultivars, thus expanding the suite of strategies for the improvement of arboreal traits and innovation within the field of forestry. Compared to diploid <i>Robinia pseudoacacia</i> L. (black locust) ‘D26-5①’ (2×), its dwarfed homologous tetraploid ‘D26-5②’ (4×) variety has better application prospects in garden vegetation guardrails and urban landscape. However, the molecular mechanism of the generation and growth of this dwarf variety is still unclear. Here, plant growth and development as well as histological differences between the diploid and its autotetraploid were investigated. Levels of endogenous hormones at three different developmental stages (20, 40, and 70 days) of 2× and homologous 4× tissue culture plantlets were assessed, and it was found that the brassinosteroid (BR) contents of the former were significantly higher than the latter. Transcriptome sequencing data analysis of 2× and homologous 4× showed that differentially expressed genes (DEGs) were significantly enriched in plant hormone synthesis and signal transduction, sugar and starch metabolism, and the plant circadian rhythm pathway, which are closely related to plant growth and development. Therefore, these biological pathways may be important regulatory pathways leading to dwarfism and slow growth in tetraploids. Additionally, utilizing weighted gene coexpression network analysis (WGCNA), we identified three crucial differentially expressed genes (DEGs)—<i>PRR5, CYP450</i>, and <i>SPA1</i>—that potentially underlie the observed ploidy variation. This study provides a new reference for the molecular mechanism of dwarfism in dwarfed autotetraploid black locusts. Collectively, our results of metabolite analysis and comparative transcriptomics confirm that plant hormone signaling and the circadian rhythm pathway result in dwarfism in black locusts.
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spelling doaj.art-3d49e3401c684623ad62adb1fe185d9a2024-01-29T13:59:36ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-01-01252131210.3390/ijms25021312Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.Yue Wu0Qi Guo1Cui Long2Yousry A. El-Kassaby3Yuhan Sun4Yun Li5State Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaDepartment of Forest and Conservation Sciences Faculty of Forestry, The University of British Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4, CanadaState Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaPolyploid breeding techniques aid in the cultivation of new forestry cultivars, thus expanding the suite of strategies for the improvement of arboreal traits and innovation within the field of forestry. Compared to diploid <i>Robinia pseudoacacia</i> L. (black locust) ‘D26-5①’ (2×), its dwarfed homologous tetraploid ‘D26-5②’ (4×) variety has better application prospects in garden vegetation guardrails and urban landscape. However, the molecular mechanism of the generation and growth of this dwarf variety is still unclear. Here, plant growth and development as well as histological differences between the diploid and its autotetraploid were investigated. Levels of endogenous hormones at three different developmental stages (20, 40, and 70 days) of 2× and homologous 4× tissue culture plantlets were assessed, and it was found that the brassinosteroid (BR) contents of the former were significantly higher than the latter. Transcriptome sequencing data analysis of 2× and homologous 4× showed that differentially expressed genes (DEGs) were significantly enriched in plant hormone synthesis and signal transduction, sugar and starch metabolism, and the plant circadian rhythm pathway, which are closely related to plant growth and development. Therefore, these biological pathways may be important regulatory pathways leading to dwarfism and slow growth in tetraploids. Additionally, utilizing weighted gene coexpression network analysis (WGCNA), we identified three crucial differentially expressed genes (DEGs)—<i>PRR5, CYP450</i>, and <i>SPA1</i>—that potentially underlie the observed ploidy variation. This study provides a new reference for the molecular mechanism of dwarfism in dwarfed autotetraploid black locusts. Collectively, our results of metabolite analysis and comparative transcriptomics confirm that plant hormone signaling and the circadian rhythm pathway result in dwarfism in black locusts.https://www.mdpi.com/1422-0067/25/2/1312<i>Robinia pseudoacacia</i> L.autotetraploiddwarfism typetranscriptomeplant circadian rhythm
spellingShingle Yue Wu
Qi Guo
Cui Long
Yousry A. El-Kassaby
Yuhan Sun
Yun Li
Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
International Journal of Molecular Sciences
<i>Robinia pseudoacacia</i> L.
autotetraploid
dwarfism type
transcriptome
plant circadian rhythm
title Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
title_full Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
title_fullStr Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
title_full_unstemmed Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
title_short Transcriptomic and Phenotypic Analyses Reveal the Molecular Mechanism of Dwarfing in Tetraploid <i>Robinia pseudoacacia</i> L.
title_sort transcriptomic and phenotypic analyses reveal the molecular mechanism of dwarfing in tetraploid i robinia pseudoacacia i l
topic <i>Robinia pseudoacacia</i> L.
autotetraploid
dwarfism type
transcriptome
plant circadian rhythm
url https://www.mdpi.com/1422-0067/25/2/1312
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