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Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development

BACKGROUND: Phospholipases As (PLAs) are acyl hydrolases that catalyze the release of free fatty acids in phospholipids and play multiple functions in plant growth and development. The three families of PLAs are: PLA1, PLA2 (sPLA), and patatin-related PLA (pPLA). The diverse functions that pPLAs pla...

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Autores principales: Wang, Mingyang, Tian, Dingyan, Li, Tengyu, Pan, Jingwen, Wang, Chenlei, Wu, Lanxin, Luo, Kun, Mei, Zhenyu, Liu, Jinwei, Chen, Wei, Yao, Jinbo, Li, Yan, Wang, Fuxin, Zhu, Shouhong, Zhang, Yongshan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10685517/
https://www.ncbi.nlm.nih.gov/pubmed/38017370
http://dx.doi.org/10.1186/s12870-023-04590-4
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author Wang, Mingyang
Tian, Dingyan
Li, Tengyu
Pan, Jingwen
Wang, Chenlei
Wu, Lanxin
Luo, Kun
Mei, Zhenyu
Liu, Jinwei
Chen, Wei
Yao, Jinbo
Li, Yan
Wang, Fuxin
Zhu, Shouhong
Zhang, Yongshan
author_facet Wang, Mingyang
Tian, Dingyan
Li, Tengyu
Pan, Jingwen
Wang, Chenlei
Wu, Lanxin
Luo, Kun
Mei, Zhenyu
Liu, Jinwei
Chen, Wei
Yao, Jinbo
Li, Yan
Wang, Fuxin
Zhu, Shouhong
Zhang, Yongshan
author_sort Wang, Mingyang
collection PubMed
description BACKGROUND: Phospholipases As (PLAs) are acyl hydrolases that catalyze the release of free fatty acids in phospholipids and play multiple functions in plant growth and development. The three families of PLAs are: PLA1, PLA2 (sPLA), and patatin-related PLA (pPLA). The diverse functions that pPLAs play in the growth and development of a broad range of plants have been demonstrated by prior studies. METHODS: Genome-wide analysis of the pPLA gene family and screening of genes for expression verification and gene silencing verification were conducted. Additionally, pollen vitality testing, analysis of the pollen expression pattern, and the detection of POD, SOD, CAT, MDA, and H(2)O(2) were performed. RESULT: In this study, 294 pPLAs were identified from 13 plant species, including 46 GhpPLAs that were divided into three subfamilies (I-III). Expression patterns showed that the majority of GhpPLAs were preferentially expressed in the petal, pistil, anther, and ovule, among other reproductive organs. Particularly, GhpPLA23 and GhpPLA44, were found to be potentially important for the reproductive development of G. hirsutum. Functional validation was demonstrated by VIGS which showed that reduced expression levels of GhpPLA23 and GhpPLA44 in the silenced plants were associated with a decrease in pollen activity. Moreover, a substantial shift in ROS and ROS scavengers and a considerable increase in POD, CAT, SOD, and other physiological parameters was found out in these silenced plants. Our results provide plausibility to the hypothesis that GhpPLA23 and GhpPLA44 had a major developmental impact on cotton reproductive systems. These results also suggest that pPLAs are important for G. hirsutum’s reproductive development and suggest that they could be employed as potential genes for haploid induction. CONCLUSIONS: The findings of the present research indicate that pPLA genes are essential for the development of floral organs and sperm cells in cotton. Consequently, this family might be important for the reproductive development of cotton and possibly for inducing the plant develop haploid progeny. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04590-4.
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spelling pubmed-106855172023-11-30 Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development Wang, Mingyang Tian, Dingyan Li, Tengyu Pan, Jingwen Wang, Chenlei Wu, Lanxin Luo, Kun Mei, Zhenyu Liu, Jinwei Chen, Wei Yao, Jinbo Li, Yan Wang, Fuxin Zhu, Shouhong Zhang, Yongshan BMC Plant Biol Research BACKGROUND: Phospholipases As (PLAs) are acyl hydrolases that catalyze the release of free fatty acids in phospholipids and play multiple functions in plant growth and development. The three families of PLAs are: PLA1, PLA2 (sPLA), and patatin-related PLA (pPLA). The diverse functions that pPLAs play in the growth and development of a broad range of plants have been demonstrated by prior studies. METHODS: Genome-wide analysis of the pPLA gene family and screening of genes for expression verification and gene silencing verification were conducted. Additionally, pollen vitality testing, analysis of the pollen expression pattern, and the detection of POD, SOD, CAT, MDA, and H(2)O(2) were performed. RESULT: In this study, 294 pPLAs were identified from 13 plant species, including 46 GhpPLAs that were divided into three subfamilies (I-III). Expression patterns showed that the majority of GhpPLAs were preferentially expressed in the petal, pistil, anther, and ovule, among other reproductive organs. Particularly, GhpPLA23 and GhpPLA44, were found to be potentially important for the reproductive development of G. hirsutum. Functional validation was demonstrated by VIGS which showed that reduced expression levels of GhpPLA23 and GhpPLA44 in the silenced plants were associated with a decrease in pollen activity. Moreover, a substantial shift in ROS and ROS scavengers and a considerable increase in POD, CAT, SOD, and other physiological parameters was found out in these silenced plants. Our results provide plausibility to the hypothesis that GhpPLA23 and GhpPLA44 had a major developmental impact on cotton reproductive systems. These results also suggest that pPLAs are important for G. hirsutum’s reproductive development and suggest that they could be employed as potential genes for haploid induction. CONCLUSIONS: The findings of the present research indicate that pPLA genes are essential for the development of floral organs and sperm cells in cotton. Consequently, this family might be important for the reproductive development of cotton and possibly for inducing the plant develop haploid progeny. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04590-4. BioMed Central 2023-11-29 /pmc/articles/PMC10685517/ /pubmed/38017370 http://dx.doi.org/10.1186/s12870-023-04590-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wang, Mingyang
Tian, Dingyan
Li, Tengyu
Pan, Jingwen
Wang, Chenlei
Wu, Lanxin
Luo, Kun
Mei, Zhenyu
Liu, Jinwei
Chen, Wei
Yao, Jinbo
Li, Yan
Wang, Fuxin
Zhu, Shouhong
Zhang, Yongshan
Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title_full Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title_fullStr Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title_full_unstemmed Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title_short Comprehensive identification and functional characterization of GhpPLA gene family in reproductive organ development
title_sort comprehensive identification and functional characterization of ghppla gene family in reproductive organ development
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10685517/
https://www.ncbi.nlm.nih.gov/pubmed/38017370
http://dx.doi.org/10.1186/s12870-023-04590-4
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