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The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii

Tree stems undergo a massive secondary growth in which secondary xylem and phloem tissues arise from the vascular cambium. Vascular cambium activity is driven by endogenous developmental signalling cues and environmental stimuli. Current knowledge regarding the genetic regulation of cambium activity...

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Autores principales: Shen, Defeng, Holmer, Rens, Kulikova, Olga, Mannapperuma, Chanaka, Street, Nathaniel R., Yan, Zhichun, van der Maden, Thomas, Bu, Fengjiao, Zhang, Yuanyuan, Geurts, Rene, Magne, Kévin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9543857/
https://www.ncbi.nlm.nih.gov/pubmed/33735477
http://dx.doi.org/10.1111/tpj.15242
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author Shen, Defeng
Holmer, Rens
Kulikova, Olga
Mannapperuma, Chanaka
Street, Nathaniel R.
Yan, Zhichun
van der Maden, Thomas
Bu, Fengjiao
Zhang, Yuanyuan
Geurts, Rene
Magne, Kévin
author_facet Shen, Defeng
Holmer, Rens
Kulikova, Olga
Mannapperuma, Chanaka
Street, Nathaniel R.
Yan, Zhichun
van der Maden, Thomas
Bu, Fengjiao
Zhang, Yuanyuan
Geurts, Rene
Magne, Kévin
author_sort Shen, Defeng
collection PubMed
description Tree stems undergo a massive secondary growth in which secondary xylem and phloem tissues arise from the vascular cambium. Vascular cambium activity is driven by endogenous developmental signalling cues and environmental stimuli. Current knowledge regarding the genetic regulation of cambium activity and secondary growth is still far from complete. The tropical Cannabaceae tree Parasponia andersonii is a non‐legume research model of nitrogen‐fixing root nodulation. Parasponia andersonii can be transformed efficiently, making it amenable for CRISPR‐Cas9‐mediated reverse genetics. We considered whether P. andersonii also could be used as a complementary research system to investigate tree‐related traits, including secondary growth. We established a developmental map of stem secondary growth in P. andersonii plantlets. Subsequently, we showed that the expression of the co‐transcriptional regulator PanNODULE ROOT1 (PanNOOT1) is essential for controlling this process. PanNOOT1 is orthologous to Arabidopsis thaliana BLADE‐ON‐PETIOLE1 (AtBOP1) and AtBOP2, which are involved in the meristem‐to‐organ‐boundary maintenance. Moreover, in species forming nitrogen‐fixing root nodules, NOOT1 is known to function as a key nodule identity gene. Parasponia andersonii CRISPR‐Cas9 loss‐of‐function Pannoot1 mutants are altered in the development of the xylem and phloem tissues without apparent disturbance of the cambium organization and size. Transcriptomic analysis showed that the expression of key secondary growth‐related genes is significantly down‐regulated in Pannoot1 mutants. This allows us to conclude that PanNOOT1 positively contributes to the regulation of stem secondary growth. Our work also demonstrates that P. andersonii can serve as a tree research system.
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spelling pubmed-95438572022-10-14 The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii Shen, Defeng Holmer, Rens Kulikova, Olga Mannapperuma, Chanaka Street, Nathaniel R. Yan, Zhichun van der Maden, Thomas Bu, Fengjiao Zhang, Yuanyuan Geurts, Rene Magne, Kévin Plant J Original Articles Tree stems undergo a massive secondary growth in which secondary xylem and phloem tissues arise from the vascular cambium. Vascular cambium activity is driven by endogenous developmental signalling cues and environmental stimuli. Current knowledge regarding the genetic regulation of cambium activity and secondary growth is still far from complete. The tropical Cannabaceae tree Parasponia andersonii is a non‐legume research model of nitrogen‐fixing root nodulation. Parasponia andersonii can be transformed efficiently, making it amenable for CRISPR‐Cas9‐mediated reverse genetics. We considered whether P. andersonii also could be used as a complementary research system to investigate tree‐related traits, including secondary growth. We established a developmental map of stem secondary growth in P. andersonii plantlets. Subsequently, we showed that the expression of the co‐transcriptional regulator PanNODULE ROOT1 (PanNOOT1) is essential for controlling this process. PanNOOT1 is orthologous to Arabidopsis thaliana BLADE‐ON‐PETIOLE1 (AtBOP1) and AtBOP2, which are involved in the meristem‐to‐organ‐boundary maintenance. Moreover, in species forming nitrogen‐fixing root nodules, NOOT1 is known to function as a key nodule identity gene. Parasponia andersonii CRISPR‐Cas9 loss‐of‐function Pannoot1 mutants are altered in the development of the xylem and phloem tissues without apparent disturbance of the cambium organization and size. Transcriptomic analysis showed that the expression of key secondary growth‐related genes is significantly down‐regulated in Pannoot1 mutants. This allows us to conclude that PanNOOT1 positively contributes to the regulation of stem secondary growth. Our work also demonstrates that P. andersonii can serve as a tree research system. John Wiley and Sons Inc. 2021-04-07 2021-06 /pmc/articles/PMC9543857/ /pubmed/33735477 http://dx.doi.org/10.1111/tpj.15242 Text en © 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Articles
Shen, Defeng
Holmer, Rens
Kulikova, Olga
Mannapperuma, Chanaka
Street, Nathaniel R.
Yan, Zhichun
van der Maden, Thomas
Bu, Fengjiao
Zhang, Yuanyuan
Geurts, Rene
Magne, Kévin
The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title_full The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title_fullStr The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title_full_unstemmed The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title_short The BOP‐type co‐transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii
title_sort bop‐type co‐transcriptional regulator nodule root1 promotes stem secondary growth of the tropical cannabaceae tree parasponia andersonii
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9543857/
https://www.ncbi.nlm.nih.gov/pubmed/33735477
http://dx.doi.org/10.1111/tpj.15242
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