Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants

The stable expression of transgenes was critically influenced by post-transcriptional regulatory mechanisms in transgenic plants. In this study, we investigated the influence of endogenous miRNA-mediated silencing on heterologous gene expression by introducing walnut (Juglans regia L.)-derived Growt...

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Main Authors: Baoxin Li, Mengting Pan, Dezheng Wu, Zhimin Zheng, Dong Pei
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1629166/full
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author Baoxin Li
Mengting Pan
Dezheng Wu
Zhimin Zheng
Dong Pei
author_facet Baoxin Li
Mengting Pan
Dezheng Wu
Zhimin Zheng
Dong Pei
author_sort Baoxin Li
collection DOAJ
description The stable expression of transgenes was critically influenced by post-transcriptional regulatory mechanisms in transgenic plants. In this study, we investigated the influence of endogenous miRNA-mediated silencing on heterologous gene expression by introducing walnut (Juglans regia L.)-derived Growth-Regulating Factors 4 (JrGRF4b), disrupting miR396-mediated silencing of replace-JrGRF4b (rJrGRF4b), and Jr-miR396a into birch (Betula platyphylla Suk.). While JrGRF4b overexpression showed no significant improvement in transformation efficiency due to Bp-miR396-mediated suppression, transgenic lines expressing rJrGRF4b exhibited a 2.53% increase in transformation efficiency, along with significantly enhanced callus diameter, adventitious bud height, root elongation, cellular expansion, and shoot primordia proliferation compared to control (**p<0.01). In contrast, Jr-miR396a-overexpressing plants displayed growth inhibition through suppression of endogenous BpGRFs. The results showed that escaping endogenous miRNA regulation by targeted site modification of rJrGRF4b significantly improved transgene performance in woody plants. Thus, comprehensive evaluation of post-transcriptional epigenetic regulation between transgenes and endogenous miRNAs in recipient plants was demonstrated to be important, and targeted escape from such miRNA-mediated suppression was shown to ensure stable and high-efficiency transgene expression.
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issn 1664-462X
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publisher Frontiers Media S.A.
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series Frontiers in Plant Science
spelling doaj-art-b6bd3bbddee4407d884be879904b43e12025-08-20T03:22:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-06-011610.3389/fpls.2025.16291661629166Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plantsBaoxin Li0Mengting Pan1Dezheng Wu2Zhimin Zheng3Dong Pei4State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, ChinaState Key Laboratory of Tree Genetics and Breeding, College of Forestry, Northeast Forestry University, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, ChinaState Key Laboratory of Tree Genetics and Breeding, College of Forestry, Northeast Forestry University, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, ChinaThe stable expression of transgenes was critically influenced by post-transcriptional regulatory mechanisms in transgenic plants. In this study, we investigated the influence of endogenous miRNA-mediated silencing on heterologous gene expression by introducing walnut (Juglans regia L.)-derived Growth-Regulating Factors 4 (JrGRF4b), disrupting miR396-mediated silencing of replace-JrGRF4b (rJrGRF4b), and Jr-miR396a into birch (Betula platyphylla Suk.). While JrGRF4b overexpression showed no significant improvement in transformation efficiency due to Bp-miR396-mediated suppression, transgenic lines expressing rJrGRF4b exhibited a 2.53% increase in transformation efficiency, along with significantly enhanced callus diameter, adventitious bud height, root elongation, cellular expansion, and shoot primordia proliferation compared to control (**p<0.01). In contrast, Jr-miR396a-overexpressing plants displayed growth inhibition through suppression of endogenous BpGRFs. The results showed that escaping endogenous miRNA regulation by targeted site modification of rJrGRF4b significantly improved transgene performance in woody plants. Thus, comprehensive evaluation of post-transcriptional epigenetic regulation between transgenes and endogenous miRNAs in recipient plants was demonstrated to be important, and targeted escape from such miRNA-mediated suppression was shown to ensure stable and high-efficiency transgene expression.https://www.frontiersin.org/articles/10.3389/fpls.2025.1629166/fullwalnutbirchMiR396growth-regulating factorspost-transcriptional regulatorytransgene
spellingShingle Baoxin Li
Mengting Pan
Dezheng Wu
Zhimin Zheng
Dong Pei
Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
Frontiers in Plant Science
walnut
birch
MiR396
growth-regulating factors
post-transcriptional regulatory
transgene
title Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
title_full Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
title_fullStr Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
title_full_unstemmed Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
title_short Escaping endogenous miRNA post-transcriptional silencing of JrGRF4b enhanced transformation efficiency in woody plants
title_sort escaping endogenous mirna post transcriptional silencing of jrgrf4b enhanced transformation efficiency in woody plants
topic walnut
birch
MiR396
growth-regulating factors
post-transcriptional regulatory
transgene
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1629166/full
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AT dezhengwu escapingendogenousmirnaposttranscriptionalsilencingofjrgrf4benhancedtransformationefficiencyinwoodyplants
AT zhiminzheng escapingendogenousmirnaposttranscriptionalsilencingofjrgrf4benhancedtransformationefficiencyinwoodyplants
AT dongpei escapingendogenousmirnaposttranscriptionalsilencingofjrgrf4benhancedtransformationefficiencyinwoodyplants