Cargando…

GhFAD2–3 is required for anther development in Gossypium hirsutum

BACKGROUND: In higher plants, the FAD2 gene encodes the microsomal oleate (Δ12)-desaturase, one of the key enzymes essential for the biosynthesis of the polyunsaturated lipids that serve many important functions in plant development and stress responses. FAD2 catalyzes the first step, in the biosynt...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Feng, Ma, Lihong, Wang, Youwu, Li, Yanjun, Zhang, Xinyu, Xue, Fei, Nie, Xinhui, Zhu, Qianhao, Sun, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6734329/
https://www.ncbi.nlm.nih.gov/pubmed/31500565
http://dx.doi.org/10.1186/s12870-019-2010-9
_version_ 1783450132474232832
author Liu, Feng
Ma, Lihong
Wang, Youwu
Li, Yanjun
Zhang, Xinyu
Xue, Fei
Nie, Xinhui
Zhu, Qianhao
Sun, Jie
author_facet Liu, Feng
Ma, Lihong
Wang, Youwu
Li, Yanjun
Zhang, Xinyu
Xue, Fei
Nie, Xinhui
Zhu, Qianhao
Sun, Jie
author_sort Liu, Feng
collection PubMed
description BACKGROUND: In higher plants, the FAD2 gene encodes the microsomal oleate (Δ12)-desaturase, one of the key enzymes essential for the biosynthesis of the polyunsaturated lipids that serve many important functions in plant development and stress responses. FAD2 catalyzes the first step, in the biosynthesis of the polyunsaturated fatty acids (PUFAs) found in the cell membrane and cell wall, and it is thus of great importance to investigate the regulatory role of FAD2 in anther development. RESULTS: We reported the molecular characterization of the cotton (Gossypium hirsutum) GhFAD2 gene family and the essential role of GhFAD2–3 in cotton anther development. G. hirsutum contains four pairs of homoeologous FAD2 genes (GhFAD2–1 to GhFAD2–4). GhFAD2–3 is ubiquitously and relatively highly expressed in all analyzed tissues, particularly in anthers. Specific inhibition of GhFAD2–3 using the RNA interference approach resulted in male sterility due to impaired anther development at the stages from meiosis to maturation. The cellular phenotypic abnormality observed at the meiosis stage of the GhFAD2–3 silenced plant (fad2–3) coincides with the significant reduction of C18:2 in anthers at the same stage. Compared with that of the wild type (WT), the content of C18:1 was 41.48%, which increased by 5 fold in the fad2–3 anther at the pollen maturation stage. Moreover, the ratio of monounsaturated to polyunsaturated fatty acid was 5.43 in fad2–3 anther, which was much higher than that of the WT (only 0.39). Through compositional analysis of anthers cuticle and transcriptome data, we demonstrated it was unfavorable to the development of anther by regulating GhFAD2–3 expression level to increase the oleic acid content. CONCLUSIONS: Our work demonstrated the importance of C18:2 and/or C18:3 in the development of the pollen exine and anther cuticle in cotton and provided clue for further investigation of the physiological significance of the fatty acid composition for plant growth and development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-2010-9) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6734329
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-67343292019-09-12 GhFAD2–3 is required for anther development in Gossypium hirsutum Liu, Feng Ma, Lihong Wang, Youwu Li, Yanjun Zhang, Xinyu Xue, Fei Nie, Xinhui Zhu, Qianhao Sun, Jie BMC Plant Biol Research Article BACKGROUND: In higher plants, the FAD2 gene encodes the microsomal oleate (Δ12)-desaturase, one of the key enzymes essential for the biosynthesis of the polyunsaturated lipids that serve many important functions in plant development and stress responses. FAD2 catalyzes the first step, in the biosynthesis of the polyunsaturated fatty acids (PUFAs) found in the cell membrane and cell wall, and it is thus of great importance to investigate the regulatory role of FAD2 in anther development. RESULTS: We reported the molecular characterization of the cotton (Gossypium hirsutum) GhFAD2 gene family and the essential role of GhFAD2–3 in cotton anther development. G. hirsutum contains four pairs of homoeologous FAD2 genes (GhFAD2–1 to GhFAD2–4). GhFAD2–3 is ubiquitously and relatively highly expressed in all analyzed tissues, particularly in anthers. Specific inhibition of GhFAD2–3 using the RNA interference approach resulted in male sterility due to impaired anther development at the stages from meiosis to maturation. The cellular phenotypic abnormality observed at the meiosis stage of the GhFAD2–3 silenced plant (fad2–3) coincides with the significant reduction of C18:2 in anthers at the same stage. Compared with that of the wild type (WT), the content of C18:1 was 41.48%, which increased by 5 fold in the fad2–3 anther at the pollen maturation stage. Moreover, the ratio of monounsaturated to polyunsaturated fatty acid was 5.43 in fad2–3 anther, which was much higher than that of the WT (only 0.39). Through compositional analysis of anthers cuticle and transcriptome data, we demonstrated it was unfavorable to the development of anther by regulating GhFAD2–3 expression level to increase the oleic acid content. CONCLUSIONS: Our work demonstrated the importance of C18:2 and/or C18:3 in the development of the pollen exine and anther cuticle in cotton and provided clue for further investigation of the physiological significance of the fatty acid composition for plant growth and development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-2010-9) contains supplementary material, which is available to authorized users. BioMed Central 2019-09-10 /pmc/articles/PMC6734329/ /pubmed/31500565 http://dx.doi.org/10.1186/s12870-019-2010-9 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Liu, Feng
Ma, Lihong
Wang, Youwu
Li, Yanjun
Zhang, Xinyu
Xue, Fei
Nie, Xinhui
Zhu, Qianhao
Sun, Jie
GhFAD2–3 is required for anther development in Gossypium hirsutum
title GhFAD2–3 is required for anther development in Gossypium hirsutum
title_full GhFAD2–3 is required for anther development in Gossypium hirsutum
title_fullStr GhFAD2–3 is required for anther development in Gossypium hirsutum
title_full_unstemmed GhFAD2–3 is required for anther development in Gossypium hirsutum
title_short GhFAD2–3 is required for anther development in Gossypium hirsutum
title_sort ghfad2–3 is required for anther development in gossypium hirsutum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6734329/
https://www.ncbi.nlm.nih.gov/pubmed/31500565
http://dx.doi.org/10.1186/s12870-019-2010-9
work_keys_str_mv AT liufeng ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT malihong ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT wangyouwu ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT liyanjun ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT zhangxinyu ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT xuefei ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT niexinhui ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT zhuqianhao ghfad23isrequiredforantherdevelopmentingossypiumhirsutum
AT sunjie ghfad23isrequiredforantherdevelopmentingossypiumhirsutum