Identification of FRL Gene Family，Expression Analysis and Functional Study of BrcFRI1 in Non-Heading Chinese Cabbage

doi:10.16420/j.issn.0513-353x.2024-1054

Acta Horticulturae Sinica ›› 2026, Vol. 53 ›› Issue (4): 1125-1142.doi: 10.16420/j.issn.0513-353x.2024-1054

• Genetic & Breeding · Germplasm Resources · Molecular Biology • Previous Articles Next Articles

Identification of FRL Gene Family，Expression Analysis and Functional Study of BrcFRI1 in Non-Heading Chinese Cabbage

BAI Xueying, TANG Manzhi, QU Tianhui, ZHANG Liting, XIAO Dong, LI Ying, HOU Xilin, LIU Tongkun^*()

Sanya Research Institute of Nanjing Agricultural University，Sanya，Hainan 572025，China

Received:2025-11-23 Revised:2025-12-31 Online:2026-04-25 Published:2026-04-20
Contact: LIU Tongkun

Abstract

Abstract:

In order to understand the functions of the FRIGIDA-Like（FRL）gene family members in non-heading Chinese cabbage，their basic properties，evolutionary characteristics，and expression features at different times and under different abiotic stresses were analyzed. Bioinformatics methods were used to identify and analyze the FRL gene family in the genome of non-heading Chinese cabbage‘NHCC001'，and transcriptome data were used to analyze the expression patterns of non-heading Chinese cabbage FRL genes under ABA treatment，and qRT-PCR was used to analyze the expression patterns under drought stress and in different periods of early and late flowering materials and three flowering genes in wild-type and transgenic Arabidopsis thaliana. The results showed that the non-heading cabbage contained a total of 13 BrcFRLs randomly distributed on seven chromosomes，and the BrcFRLs could be classified into six subgroups. The covariance analysis of five cruciferous species revealed that the FRL genes were not completely on the covariance region，and different degrees of differentiation might have occurred during the evolutionary process. In addition，cruciferae FRLs were highly expressed mainly in roots compared to species of other families，and there was differential tissue expression of BrcFRLs. cis-acting element analysis showed that all BrcFRLs contained ABA response elements，and all 11 BrcFRL members showed different degrees of response to ABA signaling，which may be regulated by ABA. Under drought stress，BrcFRL1，BrcFRI2，and BrcFRI3-1 responded significantly. BrcFRL1 was both positively regulated by ABA treatment and responsive to drought stress，suggesting that the FRL genes may be related to the hormonal response of non-heading Chinese cabbage and that ABA-responsive genes may be induced by drought stress. Overexpression of BrcFRI1 delays flowering in Arabidopsis. However，the expression of FRI and FLC in Brassica was not consistent with that in Arabidopsis，with BrcFRI accumulating in the pre-vernalization period to inhibit flowering；its expression level decreases during the vernalization process and rises again after vernalization ends. In this study，a total of 13 non-heading Chinese cabbage FRL family genes were identified，clarified the function of BrcFRL1 in delaying flowering time，and screened out a number of key genes that are related to flowering and involved in drought stress response.

Key words: non-heading Chinese cabbage, plant molecular biology, gene family, flowering time regulation, expression analysis, abiotic stress

BAI Xueying, TANG Manzhi, QU Tianhui, ZHANG Liting, XIAO Dong, LI Ying, HOU Xilin, LIU Tongkun. Identification of FRL Gene Family，Expression Analysis and Functional Study of BrcFRI1 in Non-Heading Chinese Cabbage[J]. Acta Horticulturae Sinica, 2026, 53(4): 1125-1142.

Figures/Tables 13

Table 1 Primer sequences used for qRT-PCR analysis in this study

基因 Gene	正向引物序列（5′-3′） Forward primer	反向引物序列（5′-3′） Reverse primer
ACTIN2	GTTCCAGCCCTCGTTTGTG	CAAGTGCTGTGATTTCTTTGCTC
At-FRI	GGTGCTTTGAAGCGGTCACAGT	GCCCTCTCAAATGACTCCTTGC
At-FLC	TACAGCTTCTCCTCCGGCGATA	TCCCACAAGCTTGCTATCCACA
At-FT	GGTTGGTGACTGATATCCC	GGAAGGCCGAGATTGTATAG
Brc-Actin	CTCAGTCCAAAAGAGGTATTCT	GTAGAATGTGTGATGCCAGATC
BrcFRI1	ATGGCCGTCCGTAATGGTTC	AAGACCGCATTGGAGGAATG
BrcFRI2	GGCCTTTCGTAATGGTTCTC	CAAAATCAGGTCTCCTCGTA
BrcFRL1	ATCACACCGCTCTCTCCTCT	ACCTAACTCAAACGCTGCGA
BrcFRL3-1	GGATATGGACTCAGCAGGGC	GACAATCCAAGAGACCGGCA
BrcFRL3-2	GCCTGGACAGCAACTCTCTT	GGAGTGGCTCAACTGGGTAC
BrcFRL3-3	GTGGAAGGAACTGGAGGAGC	GGTGGTGGTGACGACTCAAT
BrcFRL4-1	TCACCACGCTTGAGGAGAAC	AACGCTCGGAGTAACAAGCA
BrcFRL4-2	AGGAAGTCGCGGTTGATTGT	GCTGGCTCTGGTTCTCTTGT
BrcFLC	CCGCAAGCCTATCTCTAACC	CAGAGGAGTTTACAGAAAGCAGA
BrcFT	ACGAGAGTCCAAGGCCCAAC	TGGCGCCATCCTGGTTCATA

Table 2 Physicochemical properties of non-heading Chinese cabbage FRL gene family members

基因名称 Gene	基因号 Gene number	CDS长度/bp CDS length	氨基酸长度 Protein length	分子量 Molecular weigh	等电点 Isoelectric point	亲水性 Gravy	不稳定性指数 Instability Index
BrcFRI1	BraC03g015970.1	1 791	596	66 693.58	7.64	-0.48	70.28
BrcFRI2	BraC10g009270.1	1 710	569	63 390.88	9.14	-0.42	67.68
BrcFRL1	BraC10g024850.1	1 374	457	51 253.90	7.62	-0.50	52.23
BrcFRL2	BraC09g038630.1	1 386	461	51 418.23	9.04	-0.32	58.87
BrcFRL3-1	BraC02g041830.1	1 659	552	61 499.29	5.77	-0.41	52.56
BrcFRL3-2	BraC06g042450.1	1 140	379	41 594.13	6.42	-0.21	60.23
BrcFRL3-3	BraC09g003460.1	1 563	520	58 366.95	7.14	-0.56	58.92
BrcFRL4-1	BraC01g035560.1	1 605	534	59 035.71	6.53	-0.44	57.25
BrcFRL4-2	BraC05g030410.1	1 380	459	51 512.32	6.08	-0.40	52.40
BrcFRL5-1	BraC06g040730.1	2 595	864	96 375.21	7.73	-0.43	39.23
BrcFRL5-2	BraC09g004180.1	2 523	840	95 082.19	6.86	-0.48	37.41
BrcFRL6	BraC06g040740.1	3 471	1 156	131 268.90	5.65	-0.59	47.73
BrcFRL7	BraC09g004160.1	3 420	1 139	130 221.60	5.21	-0.57	49.36

Fig. 1 Systematic evolution and diversity analysis of the FRL gene family in cruciferous species A：Phylogenetic tree of FRL proteins constructed based on the maximum likelihood method. The species include Arabidopsis thaliana，Brassica rapa ssp. chinensis，B. rapa ssp. pekinensis，B. oleracea，and B. napus；B：Distribution of FRL genes in different subgroups（Ⅰ- Ⅵ） among the five species；C：Analysis of nucleotide differences between different subgroups

Fig. 2 Collinearity of FRL genes among five cruciferous species

Fig. 3 Chromosomal localization of the FRL genes in non-heading Chinese cabbage（Brc）and Chinese cabbage（Brp）

Fig. 4 Comprehensive analysis of the FRL gene family in Arabidopsis，non-heading Chinese cabbage，and Chinese cabbage A：Phylogenetic tree；B：Gene structure；C：Distribution of conserved motifs；D：Characteristics of the FRIGIDA domain composition

Fig. 5 Analysis of cis-acting elements in the FRL gene promoter of non-heading and Chinese cabbage

Fig. 6 Expression analysis of FRL genes in Arabidopsis thaliana，non-heading Chinese cabbage and Chinese cabbage in different tissues and before and after vernalization in Chinese cabbage

Fig. 7 Expression patterns of BrcFRI1 and BrcFRI2 at different developmental stages in early-and late-flowering non-heading cabbage varieties The different lowercase letters indicate significant differences（P < 0.05）. The same below

Fig. 8 Comparison of plant morphology（A）and flowering time（B）between wild-type（Col）and transgenic Arabidopsis

Fig. 9 Expression levels of FRI，FLC and FT genes in wild-type（Col）and BrcFRI1 transgenic Arabidopsis

Fig. 10 Time-course expression pattern of FRL genes in non-heading Chinese cabbage in response to ABA treatment

Fig. 11 Temporal expression pattern of the FRL gene in non-heading Chinese cabbage under different drought stress treatment

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Identification of FRL Gene Family，Expression Analysis and Functional Study of BrcFRI1 in Non-Heading Chinese Cabbage

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