Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars

Abstract Background In soybean, some circadian clock genes have been identified as loci for maturity traits. However, the effects of these genes on soybean circadian rhythmicity and their impacts on maturity are unclear. Results We used two geographically, phenotypically and genetically distinct cul...

Full description

Bibliographic Details
Main Authors: Yanlei Yue, Ze Jiang, Enoch Sapey, Tingting Wu, Shi Sun, Mengxue Cao, Tianfu Han, Tao Li, Hai Nian, Bingjun Jiang
Format: Article
Language:English
Published: BMC 2021-07-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-021-07869-8
_version_ 1819156671911428096
author Yanlei Yue
Ze Jiang
Enoch Sapey
Tingting Wu
Shi Sun
Mengxue Cao
Tianfu Han
Tao Li
Hai Nian
Bingjun Jiang
author_facet Yanlei Yue
Ze Jiang
Enoch Sapey
Tingting Wu
Shi Sun
Mengxue Cao
Tianfu Han
Tao Li
Hai Nian
Bingjun Jiang
author_sort Yanlei Yue
collection DOAJ
description Abstract Background In soybean, some circadian clock genes have been identified as loci for maturity traits. However, the effects of these genes on soybean circadian rhythmicity and their impacts on maturity are unclear. Results We used two geographically, phenotypically and genetically distinct cultivars, conventional juvenile Zhonghuang 24 (with functional J/GmELF3a, a homolog of the circadian clock indispensable component EARLY FLOWERING 3) and long juvenile Huaxia 3 (with dysfunctional j/Gmelf3a) to dissect the soybean circadian clock with time-series transcriptomal RNA-Seq analysis of unifoliate leaves on a day scale. The results showed that several known circadian clock components, including RVE1, GI, LUX and TOC1, phase differently in soybean than in Arabidopsis, demonstrating that the soybean circadian clock is obviously different from the canonical model in Arabidopsis. In contrast to the observation that ELF3 dysfunction results in clock arrhythmia in Arabidopsis, the circadian clock is conserved in soybean regardless of the functional status of J/GmELF3a. Soybean exhibits a circadian rhythmicity in both gene expression and alternative splicing. Genes can be grouped into six clusters, C1-C6, with different expression profiles. Many more genes are grouped into the night clusters (C4-C6) than in the day cluster (C2), showing that night is essential for gene expression and regulation. Moreover, soybean chromosomes are activated with a circadian rhythmicity, indicating that high-order chromosome structure might impact circadian rhythmicity. Interestingly, night time points were clustered in one group, while day time points were separated into two groups, morning and afternoon, demonstrating that morning and afternoon are representative of different environments for soybean growth and development. However, no genes were consistently differentially expressed over different time-points, indicating that it is necessary to perform a circadian rhythmicity analysis to more thoroughly dissect the function of a gene. Moreover, the analysis of the circadian rhythmicity of the GmFT family showed that GmELF3a might phase- and amplitude-modulate the GmFT family to regulate the juvenility and maturity traits of soybean. Conclusions These results and the resultant RNA-seq data should be helpful in understanding the soybean circadian clock and elucidating the connection between the circadian clock and soybean maturity.
first_indexed 2024-12-22T15:56:35Z
format Article
id doaj.art-475f40eb51fe46c599f7fb1a529377d8
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-12-22T15:56:35Z
publishDate 2021-07-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-475f40eb51fe46c599f7fb1a529377d82022-12-21T18:20:46ZengBMCBMC Genomics1471-21642021-07-0122111310.1186/s12864-021-07869-8Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivarsYanlei Yue0Ze Jiang1Enoch Sapey2Tingting Wu3Shi Sun4Mengxue Cao5Tianfu Han6Tao Li7Hai Nian8Bingjun Jiang9College of Life Sciences, Henan Agricultural UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural UniversityMARA Key Lab of Soybean Biology (Beijing), Institute of Crop Sciences, The Chinese Academy of Agricultural SciencesMARA Key Lab of Soybean Biology (Beijing), Institute of Crop Sciences, The Chinese Academy of Agricultural SciencesMARA Key Lab of Soybean Biology (Beijing), Institute of Crop Sciences, The Chinese Academy of Agricultural SciencesCollege of Life Sciences, Henan Agricultural UniversityMARA Key Lab of Soybean Biology (Beijing), Institute of Crop Sciences, The Chinese Academy of Agricultural SciencesCollege of Life Sciences, Henan Agricultural UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural UniversityMARA Key Lab of Soybean Biology (Beijing), Institute of Crop Sciences, The Chinese Academy of Agricultural SciencesAbstract Background In soybean, some circadian clock genes have been identified as loci for maturity traits. However, the effects of these genes on soybean circadian rhythmicity and their impacts on maturity are unclear. Results We used two geographically, phenotypically and genetically distinct cultivars, conventional juvenile Zhonghuang 24 (with functional J/GmELF3a, a homolog of the circadian clock indispensable component EARLY FLOWERING 3) and long juvenile Huaxia 3 (with dysfunctional j/Gmelf3a) to dissect the soybean circadian clock with time-series transcriptomal RNA-Seq analysis of unifoliate leaves on a day scale. The results showed that several known circadian clock components, including RVE1, GI, LUX and TOC1, phase differently in soybean than in Arabidopsis, demonstrating that the soybean circadian clock is obviously different from the canonical model in Arabidopsis. In contrast to the observation that ELF3 dysfunction results in clock arrhythmia in Arabidopsis, the circadian clock is conserved in soybean regardless of the functional status of J/GmELF3a. Soybean exhibits a circadian rhythmicity in both gene expression and alternative splicing. Genes can be grouped into six clusters, C1-C6, with different expression profiles. Many more genes are grouped into the night clusters (C4-C6) than in the day cluster (C2), showing that night is essential for gene expression and regulation. Moreover, soybean chromosomes are activated with a circadian rhythmicity, indicating that high-order chromosome structure might impact circadian rhythmicity. Interestingly, night time points were clustered in one group, while day time points were separated into two groups, morning and afternoon, demonstrating that morning and afternoon are representative of different environments for soybean growth and development. However, no genes were consistently differentially expressed over different time-points, indicating that it is necessary to perform a circadian rhythmicity analysis to more thoroughly dissect the function of a gene. Moreover, the analysis of the circadian rhythmicity of the GmFT family showed that GmELF3a might phase- and amplitude-modulate the GmFT family to regulate the juvenility and maturity traits of soybean. Conclusions These results and the resultant RNA-seq data should be helpful in understanding the soybean circadian clock and elucidating the connection between the circadian clock and soybean maturity.https://doi.org/10.1186/s12864-021-07869-8SoybeanCircadian rhythmicityTime-series transcriptomeJ/GmELF3aGmFT family
spellingShingle Yanlei Yue
Ze Jiang
Enoch Sapey
Tingting Wu
Shi Sun
Mengxue Cao
Tianfu Han
Tao Li
Hai Nian
Bingjun Jiang
Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
BMC Genomics
Soybean
Circadian rhythmicity
Time-series transcriptome
J/GmELF3a
GmFT family
title Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
title_full Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
title_fullStr Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
title_full_unstemmed Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
title_short Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars
title_sort transcriptomal dissection of soybean circadian rhythmicity in two geographically phenotypically and genetically distinct cultivars
topic Soybean
Circadian rhythmicity
Time-series transcriptome
J/GmELF3a
GmFT family
url https://doi.org/10.1186/s12864-021-07869-8
work_keys_str_mv AT yanleiyue transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT zejiang transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT enochsapey transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT tingtingwu transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT shisun transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT mengxuecao transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT tianfuhan transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT taoli transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT hainian transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars
AT bingjunjiang transcriptomaldissectionofsoybeancircadianrhythmicityintwogeographicallyphenotypicallyandgeneticallydistinctcultivars