The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa

The secondary cell wall (SCW) is essential for plant growth and development in vascular plants, and its biosynthesis is mainly controlled by a complex hierarchical regulatory network involving multiple transcription factors (TFs) at the transcription level. However, TFs that specifically regulate se...

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Main Authors: Kuan Sun, Di Fan, Yingying Peng, Chang Liu, Lingfei Kong, Ting Lan, Xianqiang Wang, Dan Li, Chaofeng Li, Keming Luo
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-05-01
Series:Horticultural Plant Journal
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Online Access:http://www.sciencedirect.com/science/article/pii/S2468014124001602
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author Kuan Sun
Di Fan
Yingying Peng
Chang Liu
Lingfei Kong
Ting Lan
Xianqiang Wang
Dan Li
Chaofeng Li
Keming Luo
author_facet Kuan Sun
Di Fan
Yingying Peng
Chang Liu
Lingfei Kong
Ting Lan
Xianqiang Wang
Dan Li
Chaofeng Li
Keming Luo
author_sort Kuan Sun
collection DOAJ
description The secondary cell wall (SCW) is essential for plant growth and development in vascular plants, and its biosynthesis is mainly controlled by a complex hierarchical regulatory network involving multiple transcription factors (TFs) at the transcription level. However, TFs that specifically regulate secondary xylem have not been widely reported. In this study, we described a poplar KNOTTED1-like homeobox (KNOX) TF PtoKNAT3a1, which was mainly expressed in the expanding xylem cells of stems. PtoKNAT3a1 overexpression caused fiber SCW thickening and increased all measured SCW compositions by upregulating the expression of SCW -biosynthetic genes and -associated TFs, but had no effect on the vessels of SCW. The opposite phenotype was observed in the PtoKNAT3a1-knockout lines. Hence, we further demonstrated that PtoKNAT3a1 could physically interact with the NAC master switches PtoWND2A/3A to enhance the expression of downstream MYB TFs and SCW biosynthetic genes (including PtoMYB20, PtoMYB21, PtoMYB90, PtoCoMT2, PtoGT43B and PtoCesA8). Meanwhile, the studies also demonstrate that the KNAT3 has functional differentiation in xylem development. Taken together, these data suggest that the KNAT3a1-WND2A/3A module positively regulates fiber development of the secondary xylem in poplar via the WND2A/3A-mediated hierarchical regulatory network, and supplies useful information for fiber SCW formation. The research not only deepens the understanding of the hierarchical regulatory network affecting SCW formation but also supplies genetic resources and molecular targets for plant fiber utilization.
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spelling doaj-art-a7f70bfff50944d8b858cd2d54f5391c2025-08-20T02:19:22ZengKeAi Communications Co., Ltd.Horticultural Plant Journal2468-01412025-05-011131326134010.1016/j.hpj.2024.05.008The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosaKuan Sun0Di Fan1Yingying Peng2Chang Liu3Lingfei Kong4Ting Lan5Xianqiang Wang6Dan Li7Chaofeng Li8Keming Luo9Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Department of Molecular Biosciences, University of Texas at Austin, Austin, TX 78705, USAChongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, ChinaMaize Research Institute, Southwest University, Chongqing 400715, China; Engineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing 400715, China; Corresponding authors.Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, China; Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing 400715, China; Corresponding authors.The secondary cell wall (SCW) is essential for plant growth and development in vascular plants, and its biosynthesis is mainly controlled by a complex hierarchical regulatory network involving multiple transcription factors (TFs) at the transcription level. However, TFs that specifically regulate secondary xylem have not been widely reported. In this study, we described a poplar KNOTTED1-like homeobox (KNOX) TF PtoKNAT3a1, which was mainly expressed in the expanding xylem cells of stems. PtoKNAT3a1 overexpression caused fiber SCW thickening and increased all measured SCW compositions by upregulating the expression of SCW -biosynthetic genes and -associated TFs, but had no effect on the vessels of SCW. The opposite phenotype was observed in the PtoKNAT3a1-knockout lines. Hence, we further demonstrated that PtoKNAT3a1 could physically interact with the NAC master switches PtoWND2A/3A to enhance the expression of downstream MYB TFs and SCW biosynthetic genes (including PtoMYB20, PtoMYB21, PtoMYB90, PtoCoMT2, PtoGT43B and PtoCesA8). Meanwhile, the studies also demonstrate that the KNAT3 has functional differentiation in xylem development. Taken together, these data suggest that the KNAT3a1-WND2A/3A module positively regulates fiber development of the secondary xylem in poplar via the WND2A/3A-mediated hierarchical regulatory network, and supplies useful information for fiber SCW formation. The research not only deepens the understanding of the hierarchical regulatory network affecting SCW formation but also supplies genetic resources and molecular targets for plant fiber utilization.http://www.sciencedirect.com/science/article/pii/S2468014124001602Fiber secondary cell wallKNAT transcription factorSecondary xylemModuleHierarchical regulatory network
spellingShingle Kuan Sun
Di Fan
Yingying Peng
Chang Liu
Lingfei Kong
Ting Lan
Xianqiang Wang
Dan Li
Chaofeng Li
Keming Luo
The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
Horticultural Plant Journal
Fiber secondary cell wall
KNAT transcription factor
Secondary xylem
Module
Hierarchical regulatory network
title The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
title_full The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
title_fullStr The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
title_full_unstemmed The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
title_short The KNAT3a1-WND2A/3A module positively regulates fiber secondary cell wall biosynthesis in Populus tomentosa
title_sort knat3a1 wnd2a 3a module positively regulates fiber secondary cell wall biosynthesis in populus tomentosa
topic Fiber secondary cell wall
KNAT transcription factor
Secondary xylem
Module
Hierarchical regulatory network
url http://www.sciencedirect.com/science/article/pii/S2468014124001602
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