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Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)

Polyploid breeding is an effective approach to improve plant biomass and quality. Both fast growth and dwarf types of in vitro or ex vitro plants are produced after polyploidization. However, little is known regarding the dwarf type mechanism in polyploids grown in vitro. In this study, the morpholo...

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Autores principales: Chen, Siyuan, Zhang, Yan, Zhang, Ting, Zhan, Dingju, Pang, Zhenwu, Zhao, Jian, Zhang, Jinfeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271929/
https://www.ncbi.nlm.nih.gov/pubmed/35832220
http://dx.doi.org/10.3389/fpls.2022.924044
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author Chen, Siyuan
Zhang, Yan
Zhang, Ting
Zhan, Dingju
Pang, Zhenwu
Zhao, Jian
Zhang, Jinfeng
author_facet Chen, Siyuan
Zhang, Yan
Zhang, Ting
Zhan, Dingju
Pang, Zhenwu
Zhao, Jian
Zhang, Jinfeng
author_sort Chen, Siyuan
collection PubMed
description Polyploid breeding is an effective approach to improve plant biomass and quality. Both fast growth and dwarf types of in vitro or ex vitro plants are produced after polyploidization. However, little is known regarding the dwarf type mechanism in polyploids grown in vitro. In this study, the morphological and cytological characteristics were measured in tetraploid and diploid hybrid sweetgum (Liquidambar styraciflua × L. formosana) with the same genetic background. RNA sequencing (RNA-Seq) was used to analyse shoot and root variations between tetraploid and diploid plants; important metabolites were validated. The results showed that the shoot and root lengths were significantly shorter in tetraploids than in diploids after 25 d of culture. Most tetraploid root cells were wider and more irregular, and the length of the meristematic zone was shorter, while tetraploid cells were significantly larger than diploid cells. Differentially expressed genes (DEGs) were significantly enriched in the plant growth and organ elongation pathways, such as plant hormone biosynthesis and signal transduction, sugar and starch metabolism, and cell cycles. Hormone biosynthesis and signal transduction genes, such as YUCCA, TAA1, GH3, SAUR, CPS, KO, KAO, GA20ox, GA3ox, BAS1 and CYCD3, which help to regulate organ elongation, were generally downregulated. The auxin, gibberellin, and brassinolide (BL) contents in roots and stems were significantly lower in tetraploids than in diploids, which may greatly contribute to slow growth in the roots and stems of tetraploid regenerated plants. Exogenous gibberellic acid (GA(3)) and indole-3-acetic acid (IAA), which induced plant cell elongation, could significantly promote growth in the stems and roots of tetraploids. In summary, comparative transcriptomics and metabolite analysis showed that the slow growth of regenerated tetraploid hybrid sweetgum was strongly related to auxin and gibberellin deficiency. Our findings provide insights into the molecular mechanisms that underlie dwarfism in allopolyploid hybrid sweetgum.
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spelling pubmed-92719292022-07-12 Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana) Chen, Siyuan Zhang, Yan Zhang, Ting Zhan, Dingju Pang, Zhenwu Zhao, Jian Zhang, Jinfeng Front Plant Sci Plant Science Polyploid breeding is an effective approach to improve plant biomass and quality. Both fast growth and dwarf types of in vitro or ex vitro plants are produced after polyploidization. However, little is known regarding the dwarf type mechanism in polyploids grown in vitro. In this study, the morphological and cytological characteristics were measured in tetraploid and diploid hybrid sweetgum (Liquidambar styraciflua × L. formosana) with the same genetic background. RNA sequencing (RNA-Seq) was used to analyse shoot and root variations between tetraploid and diploid plants; important metabolites were validated. The results showed that the shoot and root lengths were significantly shorter in tetraploids than in diploids after 25 d of culture. Most tetraploid root cells were wider and more irregular, and the length of the meristematic zone was shorter, while tetraploid cells were significantly larger than diploid cells. Differentially expressed genes (DEGs) were significantly enriched in the plant growth and organ elongation pathways, such as plant hormone biosynthesis and signal transduction, sugar and starch metabolism, and cell cycles. Hormone biosynthesis and signal transduction genes, such as YUCCA, TAA1, GH3, SAUR, CPS, KO, KAO, GA20ox, GA3ox, BAS1 and CYCD3, which help to regulate organ elongation, were generally downregulated. The auxin, gibberellin, and brassinolide (BL) contents in roots and stems were significantly lower in tetraploids than in diploids, which may greatly contribute to slow growth in the roots and stems of tetraploid regenerated plants. Exogenous gibberellic acid (GA(3)) and indole-3-acetic acid (IAA), which induced plant cell elongation, could significantly promote growth in the stems and roots of tetraploids. In summary, comparative transcriptomics and metabolite analysis showed that the slow growth of regenerated tetraploid hybrid sweetgum was strongly related to auxin and gibberellin deficiency. Our findings provide insights into the molecular mechanisms that underlie dwarfism in allopolyploid hybrid sweetgum. Frontiers Media S.A. 2022-06-27 /pmc/articles/PMC9271929/ /pubmed/35832220 http://dx.doi.org/10.3389/fpls.2022.924044 Text en Copyright © 2022 Chen, Zhang, Zhang, Zhan, Pang, Zhao and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Chen, Siyuan
Zhang, Yan
Zhang, Ting
Zhan, Dingju
Pang, Zhenwu
Zhao, Jian
Zhang, Jinfeng
Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title_full Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title_fullStr Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title_full_unstemmed Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title_short Comparative Transcriptomic, Anatomical and Phytohormone Analyses Provide New Insights Into Hormone-Mediated Tetraploid Dwarfing in Hybrid Sweetgum (Liquidambar styraciflua × L. formosana)
title_sort comparative transcriptomic, anatomical and phytohormone analyses provide new insights into hormone-mediated tetraploid dwarfing in hybrid sweetgum (liquidambar styraciflua × l. formosana)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271929/
https://www.ncbi.nlm.nih.gov/pubmed/35832220
http://dx.doi.org/10.3389/fpls.2022.924044
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