The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar

Osmotin-like proteins (OLPs) mediate defenses against abiotic and biotic stresses and fungal pathogens in plants. However, no OLPs have been functionally elucidated in poplar. Here, we report an osmotin-like protein designated <i>PdOLP1</i> from <i>Populus deltoides</i> (Mars...

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Main Authors: Shaofeng Li, Yaoxiang Zhang, Xuebing Xin, Changjun Ding, Fuling Lv, Wenjuan Mo, Yongxiu Xia, Shaoli Wang, Jingyan Cai, Lifang Sun, Manyi Du, Chenxi Dong, Xu Gao, Xinlu Dai, Jianhui Zhang, Jinshuang Sun
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/21/11/3993
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record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Shaofeng Li
Yaoxiang Zhang
Xuebing Xin
Changjun Ding
Fuling Lv
Wenjuan Mo
Yongxiu Xia
Shaoli Wang
Jingyan Cai
Lifang Sun
Manyi Du
Chenxi Dong
Xu Gao
Xinlu Dai
Jianhui Zhang
Jinshuang Sun
spellingShingle Shaofeng Li
Yaoxiang Zhang
Xuebing Xin
Changjun Ding
Fuling Lv
Wenjuan Mo
Yongxiu Xia
Shaoli Wang
Jingyan Cai
Lifang Sun
Manyi Du
Chenxi Dong
Xu Gao
Xinlu Dai
Jianhui Zhang
Jinshuang Sun
The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
International Journal of Molecular Sciences
functional mechanisms
negative regulator
<i>PdOLP1</i>
<i>Populus deltoides</i>
secondary wall biosynthesis
author_facet Shaofeng Li
Yaoxiang Zhang
Xuebing Xin
Changjun Ding
Fuling Lv
Wenjuan Mo
Yongxiu Xia
Shaoli Wang
Jingyan Cai
Lifang Sun
Manyi Du
Chenxi Dong
Xu Gao
Xinlu Dai
Jianhui Zhang
Jinshuang Sun
author_sort Shaofeng Li
title The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
title_short The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
title_full The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
title_fullStr The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
title_full_unstemmed The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar
title_sort osmotin-like protein gene<i> pdolp1</i> is involved in secondary cell wall biosynthesis during wood formation in poplar
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-06-01
description Osmotin-like proteins (OLPs) mediate defenses against abiotic and biotic stresses and fungal pathogens in plants. However, no OLPs have been functionally elucidated in poplar. Here, we report an osmotin-like protein designated <i>PdOLP1</i> from <i>Populus deltoides</i> (Marsh.). Expression analysis showed that <i>PdOLP1</i> transcripts were mainly present in immature xylem and immature phloem during vascular tissue development in <i>P</i>. <i>deltoides</i>. We conducted phenotypic, anatomical, and molecular analyses of <i>PdOLP1</i>-overexpressing lines and the <i>PdOLP1</i>-downregulated hybrid poplar 84K (<i>Populus alba</i> ×<i> Populus glandulosa</i>) (Hybrid poplar 84K PagOLP1, PagOLP2, PagOLP3 and PagOLP4 are highly homologous to <i>PdOLP1</i>, and are downregulated in <i>PdOLP1</i>-downregulated hybrid poplar 84K). The overexpression of <i>PdOLP1</i> led to a reduction in the radial width and cell layer number in the xylem and phloem zones, in expression of genes involved in lignin biosynthesis, and in the fibers and vessels of xylem cell walls in the overexpressing lines. Additionally, the xylem vessels and fibers of <i>PdOLP1</i>-downregulated poplar exhibited increased secondary cell wall thickness. Elevated expression of secondary wall biosynthetic genes was accompanied by increases in lignin content, dry weight biomass, and carbon storage in <i>PdOLP1</i>-downregulated lines. A <i>PdOLP1</i> coexpression network was constructed and showed that <i>PdOLP1 </i>was coexpressed with a large number of genes involved in secondary cell wall biosynthesis and wood development in poplar. Moreover, based on transcriptional activation assays, PtobZIP5 and PtobHLH7 activated the <i>PdOLP1 </i>promoter, whereas PtoBLH8 and PtoWRKY40 repressed it. A yeast one-hybrid (Y1H) assay confirmed interaction of PtoBLH8, PtoMYB3, and PtoWRKY40 with the <i>PdOLP</i>1 promoter in vivo. Together, our results suggest that<i> PdOLP1</i> is a negative regulator of secondary wall biosynthesis and may be valuable for manipulating secondary cell wall deposition to improve carbon fixation efficiency in tree species.
topic functional mechanisms
negative regulator
<i>PdOLP1</i>
<i>Populus deltoides</i>
secondary wall biosynthesis
url https://www.mdpi.com/1422-0067/21/11/3993
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spelling doaj-ee67414e263843f3b67034eb3e2cc0112020-11-25T03:23:06ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-06-01213993399310.3390/ijms21113993The Osmotin-Like Protein Gene<i> PdOLP1</i> Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in PoplarShaofeng Li0Yaoxiang Zhang1Xuebing Xin2Changjun Ding3Fuling Lv4Wenjuan Mo5Yongxiu Xia6Shaoli Wang7Jingyan Cai8Lifang Sun9Manyi Du10Chenxi Dong11Xu Gao12Xinlu Dai13Jianhui Zhang14Jinshuang Sun15Experimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaState Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Beijing 100091, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaDepartment of Pharmaceutical Science, Biomanufacturing Research Institute and Technology Enterprise, North Carolina Central University, Durham, NC 27707, USAExperimental Center of Forestry in North China, Chinese Academy of Forestry, Beijing 100023, ChinaOsmotin-like proteins (OLPs) mediate defenses against abiotic and biotic stresses and fungal pathogens in plants. However, no OLPs have been functionally elucidated in poplar. Here, we report an osmotin-like protein designated <i>PdOLP1</i> from <i>Populus deltoides</i> (Marsh.). Expression analysis showed that <i>PdOLP1</i> transcripts were mainly present in immature xylem and immature phloem during vascular tissue development in <i>P</i>. <i>deltoides</i>. We conducted phenotypic, anatomical, and molecular analyses of <i>PdOLP1</i>-overexpressing lines and the <i>PdOLP1</i>-downregulated hybrid poplar 84K (<i>Populus alba</i> ×<i> Populus glandulosa</i>) (Hybrid poplar 84K PagOLP1, PagOLP2, PagOLP3 and PagOLP4 are highly homologous to <i>PdOLP1</i>, and are downregulated in <i>PdOLP1</i>-downregulated hybrid poplar 84K). The overexpression of <i>PdOLP1</i> led to a reduction in the radial width and cell layer number in the xylem and phloem zones, in expression of genes involved in lignin biosynthesis, and in the fibers and vessels of xylem cell walls in the overexpressing lines. Additionally, the xylem vessels and fibers of <i>PdOLP1</i>-downregulated poplar exhibited increased secondary cell wall thickness. Elevated expression of secondary wall biosynthetic genes was accompanied by increases in lignin content, dry weight biomass, and carbon storage in <i>PdOLP1</i>-downregulated lines. A <i>PdOLP1</i> coexpression network was constructed and showed that <i>PdOLP1 </i>was coexpressed with a large number of genes involved in secondary cell wall biosynthesis and wood development in poplar. Moreover, based on transcriptional activation assays, PtobZIP5 and PtobHLH7 activated the <i>PdOLP1 </i>promoter, whereas PtoBLH8 and PtoWRKY40 repressed it. A yeast one-hybrid (Y1H) assay confirmed interaction of PtoBLH8, PtoMYB3, and PtoWRKY40 with the <i>PdOLP</i>1 promoter in vivo. Together, our results suggest that<i> PdOLP1</i> is a negative regulator of secondary wall biosynthesis and may be valuable for manipulating secondary cell wall deposition to improve carbon fixation efficiency in tree species.https://www.mdpi.com/1422-0067/21/11/3993functional mechanismsnegative regulator<i>PdOLP1</i><i>Populus deltoides</i>secondary wall biosynthesis