Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)

Abstract Background Stone-hardening stage is crucial to the development of grape seed and berry quality. A significant body of evidence supports the important roles of MicroRNAs in grape-berry development, but their specific molecular functions during grape stone-hardening stage remain unclear. Resu...

Full description

Bibliographic Details
Main Authors: Peipei Wang, Xuxian Xuan, Ziwen Su, Wenran Wang, Mostafa Abdelrahman, Songtao Jiu, Xiaowen Zhang, Zhongjie Liu, Xicheng Wang, Chen Wang, Jinggui Fang
Format: Article
Language:English
Published: BMC 2021-09-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-021-03188-y
_version_ 1818885413543084032
author Peipei Wang
Xuxian Xuan
Ziwen Su
Wenran Wang
Mostafa Abdelrahman
Songtao Jiu
Xiaowen Zhang
Zhongjie Liu
Xicheng Wang
Chen Wang
Jinggui Fang
author_facet Peipei Wang
Xuxian Xuan
Ziwen Su
Wenran Wang
Mostafa Abdelrahman
Songtao Jiu
Xiaowen Zhang
Zhongjie Liu
Xicheng Wang
Chen Wang
Jinggui Fang
author_sort Peipei Wang
collection DOAJ
description Abstract Background Stone-hardening stage is crucial to the development of grape seed and berry quality. A significant body of evidence supports the important roles of MicroRNAs in grape-berry development, but their specific molecular functions during grape stone-hardening stage remain unclear. Results Here, a total of 161 conserved and 85 species-specific miRNAs/miRNAs* (precursor) were identified in grape berries at stone-hardening stage using Solexa sequencing. Amongst them, 30 VvmiRNAs were stone-hardening stage-specific, whereas 52 exhibited differential expression profiles during berry development, potentially participating in the modulation of berry development as verified by their expression patterns. GO and KEGG pathway analysis showed that 13 VvmiRNAs might be involved in the regulation of embryo development, another 11 in lignin and cellulose biosynthesis, and also 28 in the modulation of hormone signaling, sugar, and proline metabolism. Furthermore, the target genes for 4 novel VvmiRNAs related to berry development were validated using RNA Ligase-Mediated (RLM)-RACE and Poly(A) Polymerase-Mediated (PPM)-RACE methods, and their cleavage mainly occurred at the 9th–11th sites from the 5′ ends of miRNAs at their binding regions. In view of the regulatory roles of GA in seed embryo development and stone-hardening in grape, we investigated the expression modes of VvmiRNAs and their target genes during GA-induced grape seedless-berry development, and we validated that GA induced the expression of VvmiR31-3p and VvmiR8-5p to negatively regulate the expression levels of CAFFEOYL COENZYME A-3-O-METHYLTRANSFERASE (VvCCoAOMT), and DDB1-CUL4 ASSOCIATED FACTOR1 (VvDCAF1). The series of changes might repress grape stone hardening and embryo development, which might be a potential key molecular mechanism in GA-induced grape seedless-berry development. Finally, a schematic model of miRNA-mediated grape seed and stone-hardening development was proposed. Conclusion This work identified 30 stone-hardening stage-specific VvmiRNAs and 52 significant differential expression ones, and preliminary interpreted the potential molecular mechanism of GA-induced grape parthenocarpy. GA negatively manipulate the expression of VvCCoAOMT and VvDCAF1 by up-regulation the expression of VvmiR31-3p and VvmiR8-5p, thereby repressing seed stone and embryo development to produce grape seedless berries.
first_indexed 2024-12-19T16:05:03Z
format Article
id doaj.art-cbf01fb4b50d49c4ba5edf068e082305
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-12-19T16:05:03Z
publishDate 2021-09-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-cbf01fb4b50d49c4ba5edf068e0823052022-12-21T20:14:51ZengBMCBMC Plant Biology1471-22292021-09-0121112110.1186/s12870-021-03188-yIdentification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)Peipei Wang0Xuxian Xuan1Ziwen Su2Wenran Wang3Mostafa Abdelrahman4Songtao Jiu5Xiaowen Zhang6Zhongjie Liu7Xicheng Wang8Chen Wang9Jinggui Fang10College of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityDepartment of Botany, Faculty of Sciences, Aswan UniversityDepartment of Plant Science, School of Agriculture and Biology, Shanghai Jiao Tong UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityDepartment of Plant Science, School of Agriculture and Biology, Shanghai Jiao Tong UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityAbstract Background Stone-hardening stage is crucial to the development of grape seed and berry quality. A significant body of evidence supports the important roles of MicroRNAs in grape-berry development, but their specific molecular functions during grape stone-hardening stage remain unclear. Results Here, a total of 161 conserved and 85 species-specific miRNAs/miRNAs* (precursor) were identified in grape berries at stone-hardening stage using Solexa sequencing. Amongst them, 30 VvmiRNAs were stone-hardening stage-specific, whereas 52 exhibited differential expression profiles during berry development, potentially participating in the modulation of berry development as verified by their expression patterns. GO and KEGG pathway analysis showed that 13 VvmiRNAs might be involved in the regulation of embryo development, another 11 in lignin and cellulose biosynthesis, and also 28 in the modulation of hormone signaling, sugar, and proline metabolism. Furthermore, the target genes for 4 novel VvmiRNAs related to berry development were validated using RNA Ligase-Mediated (RLM)-RACE and Poly(A) Polymerase-Mediated (PPM)-RACE methods, and their cleavage mainly occurred at the 9th–11th sites from the 5′ ends of miRNAs at their binding regions. In view of the regulatory roles of GA in seed embryo development and stone-hardening in grape, we investigated the expression modes of VvmiRNAs and their target genes during GA-induced grape seedless-berry development, and we validated that GA induced the expression of VvmiR31-3p and VvmiR8-5p to negatively regulate the expression levels of CAFFEOYL COENZYME A-3-O-METHYLTRANSFERASE (VvCCoAOMT), and DDB1-CUL4 ASSOCIATED FACTOR1 (VvDCAF1). The series of changes might repress grape stone hardening and embryo development, which might be a potential key molecular mechanism in GA-induced grape seedless-berry development. Finally, a schematic model of miRNA-mediated grape seed and stone-hardening development was proposed. Conclusion This work identified 30 stone-hardening stage-specific VvmiRNAs and 52 significant differential expression ones, and preliminary interpreted the potential molecular mechanism of GA-induced grape parthenocarpy. GA negatively manipulate the expression of VvCCoAOMT and VvDCAF1 by up-regulation the expression of VvmiR31-3p and VvmiR8-5p, thereby repressing seed stone and embryo development to produce grape seedless berries.https://doi.org/10.1186/s12870-021-03188-yGrapeSeed and stone hardening developmentGASeedless berrymiRNATarget genes
spellingShingle Peipei Wang
Xuxian Xuan
Ziwen Su
Wenran Wang
Mostafa Abdelrahman
Songtao Jiu
Xiaowen Zhang
Zhongjie Liu
Xicheng Wang
Chen Wang
Jinggui Fang
Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
BMC Plant Biology
Grape
Seed and stone hardening development
GA
Seedless berry
miRNA
Target genes
title Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
title_full Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
title_fullStr Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
title_full_unstemmed Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
title_short Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)
title_sort identification of mirnas mediated seed and stone hardening regulatory networks and their signal pathway of ga induced seedless berries in grapevine v vinifera l
topic Grape
Seed and stone hardening development
GA
Seedless berry
miRNA
Target genes
url https://doi.org/10.1186/s12870-021-03188-y
work_keys_str_mv AT peipeiwang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT xuxianxuan identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT ziwensu identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT wenranwang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT mostafaabdelrahman identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT songtaojiu identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT xiaowenzhang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT zhongjieliu identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT xichengwang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT chenwang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal
AT jingguifang identificationofmirnasmediatedseedandstonehardeningregulatorynetworksandtheirsignalpathwayofgainducedseedlessberriesingrapevinevviniferal