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Review

Advancements in Molecular Mechanism Research on Bolting Traits in Vegetable Crops

by
Guo-Fei Tan
1,2,
Qing Luo
1,2,3,
Shun-Hua Zhu
1,2,
Xiu-Lai Zhong
1,2,
Ping-Hong Meng
1,
Meng-Yao Li
4,
Zhi-Feng Chen
5,* and
Ai-Sheng Xiong
3,*
1
Institute of Horticulture, Guizhou Academy of Agricultural Sciences/Guizhou Horticultural Engineering Technology Research Center, Guiyang 550006, China
2
Key Laboratory of Crop Gene Resources and Germplasm Innovation in Karst Mountain Area of Agriculture and Rural Ministry, Guiyang 550006, China
3
State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
4
College of Horticulture, Sichuan Agricultural University, Chengdu 611130, China
5
College of Biology and Agricultural Technology, Zunyi Normal College, Zunyi 563006, China
*
Authors to whom correspondence should be addressed.
Horticulturae 2024, 10(7), 670; https://doi.org/10.3390/horticulturae10070670
Submission received: 7 May 2024 / Revised: 14 June 2024 / Accepted: 21 June 2024 / Published: 25 June 2024
(This article belongs to the Special Issue Modernizing Horticultural Crop Improvement for Enhanced Yields and Quality)
Browse Figure
Versions Notes

Abstract

:
Bolting and flowering of vegetables are induced by vernalization in their early growth stage. This phenomenon is called premature bolting, and it has caused massive losses in production of vegetables such as cabbage, celery, carrot, radish, and spinach, etc. This review aimed to summarize studies on bolting and flowering pathways, physiological and biochemical changes, and underlined molecular mechanisms of various vegetable crop bolting involving genome and transcriptome analysis, and its association with vegetable breeding. This review could provide basic knowledge to carry out research on vegetable genetics and breeding and vegetable cultivation.

1. Introduction

The flowering transition from vegetative to reproductive growth and the formation of floral organs in higher plants plays a central role in the development, reproduction, and evolution of plant species [1]. Many vegetable crops require low-temperature vernalization to produce flowers in thes early growth stage, leading to flower bud differentiation and bolting [2]. Vegetable crops undergo bolting bloom before a knotting/non-knotting ball or fleshy root/stems are formed; this process is known as early or immature bolting [3]. It affects the yield and quality of the harvested products of vegetable crops, making it an important issue for breeders, researchers, and growers to address. They must study the early and late bolting of different plants according to the different needs of various vegetable crops [4].
Vegetable crops are widely cultivated in China and other countries due to their diverse types, high nutritional value, and strong adaptability. Although extensive research has been conducted on the bolting of vegetable crops worldwide, the most common subjects are leafy vegetables, including cabbage (Brassica oleracea L.) [5,6], turnip (Brassica rapa L.) [7], Chinese cabbage (Brassica campestris L.) [8], mustard (Brassica juncea L.) [9], celery (Apium graveolens L.) [10,11,12,13], lettuce (Lactuca sativa L.) [14], and spinach (Spinacia oleracea L.) [15]; succulent root vegetables such as carrot (Daucus carota L.) [16,17,18,19,20] and radish (Raphanus sativus L.) [21]; vegetable liverworts such as B. rapa var. chinensis ‘Parachinensis’ [22]; and bulbous vegetables such as onion (Allium cepa L.) [23] and garlic (Allium sativum L.) [24] (Figure 1a).
To date, information obtained from germplasm resources through physiological and molecular research on various vegetable crops is limited. This review aims to summarize studies on environmental factors, physiological and biochemical changes, breeding, and molecular mechanisms in commonly used vegetable crops. We sincerely hope that this review can provide useful theoretical and practical information to assist research on bolting.

2. Bolting and Flowering Factors

2.1. Preconditions

During the transition from the vegetative growth stage to the reproductive growth stage, plants must go through a period of continuous low temperature, known as vernalization. This is a crucial process for the formation of flower organs and the regulation of flowering. The preconditions for bolting include seed vernalization [10,25,26,27], plumulevernalization [28,29,30], devernalization [31,32], vernalization [1,2,33], and non-vernalization [34]. Liliaceae crops, such as garlic and scallion, and Apiaceae crops, such as carrot and celery, undergo plumule vernalization. Amaranthaceae crops, including spinach, and Brassicaceae crops, such as radish, Chinese cabbage, choy sum (B. campestris L. ssp. chinensis var. utilis Tsen et Lee), turnip, and mustard, primarily undergo seedvernalization. In contrast, crops like red liverwort, liverwort, and pakchoi exhibit non-vernalization [6]. Compositae crops, including asparagus lettuce, garland chrysanthemum, and lettuce, undergo devernalization (Figure 1a).

2.2. Bolting and Flowering Pathways

Bolting, defined as stem elongation, is a prerequisite for flowering. Changes in environmental conditions, such as vernalization temperature and light, can lead to immature bolting in many vegetable crops, which reduces productivity and commercial value [8,35,36]. To understand the molecular mechanisms underlying floral transition, extensive research has been conducted on model plants [37]. This research has identified six flowering regulatory pathways mediated by photoreceptor-mediated environmental signaling in Arabidopsis thaliana: vernalization [1,38], photoperiodic [1,39,40], temperature [24], gibberellins (GAs) [14], autonomous [41], and age pathway [42] (Figure 1b).

2.3. Vernalization and Devernalization Pathway

A low temperature promotes flower bud differentiation and flowering in vegetables such as celery [10], carrot [16,43], garlic [24], and wild lettuce (Lactuca georgica) [44]. Michael et al. [45] proposed that favorable temperatures could replace the photoperiod requirements for garlic, facilitating meristem transition, flowering, and bulbing under suboptimal photoperiod conditions. Suitable temperatures are another key factor inducing bolting and flowering in vegetable crops. High temperatures can induce early bolting, affecting both quality and production in crops like lettuce [44] and garlic [46].
Photoperiod pathway: Premature bolting in long-day plants such as Chinese cabbage [47], carrot [43,47], celery [48], and garlic [49] can be induced by extended light periods. Longer light durations are particularly beneficial for bolting in spinach and garlic [49].
Gibberellin (GA) pathway: GAs play a significant role in bolting regulation. In lettuce, for example, the expression of BcSOC1 is significantly upregulated under exogenous GA3 and low-temperature treatments, leading to early bolting and flowering in Chinese cabbage [50,51].
Other factors: The sowing time of some vegetable crops can influence the bolting time and rate. Earlier sowing times lead to older plant leaves and higher bolting rates, as observed in carrots [44]. Mero and Honma [52] found a correlation between the number of true leaves and the bolting rate in kale.

3. Physiological and Biochemical Changes before and after Bolting

Many researchers have studied the physiological and biochemical changes before and after bud formation and bolting in plants, focusing on aspects such as carbohydrates, soluble proteins, endogenous hormones, and enzyme activity to theoretically explain the bolting mechanism [53,54].

3.1. Carbohydrates

The carbohydrate mechanism in stem tips is closely related to vernalization and flower bud differentiation. High sugar levels in vernalized vegetable crops may accelerate flower initiation and development. In radish [55] and lettuce [14], the total soluble sugar content increases during the initial stages of floral bud differentiation before decreasing. Many researchers have identified a high sugar/carbohydrate ratio as a major determinant of the flowering process, as confirmed in studies on pakchoi [56]. Dai et al. [57] revealed that early bolting and faster flowering were caused by polysaccharide and sugar/carbohydrate metabolism.

3.2. Soluble Proteins

Studies have found that low total nitrogen content and high soluble protein content in vegetable crops, such as radish [54], facilitate vernalization, which is crucial for the transition to the reproductive phase. Han et al. [14] identified 30 differentially accumulated proteins using proteomic analysis of bolting-resistant and bolting-sensitive lettuce lines. Wang et al. [58] demonstrated that soluble protein (S-Pr) plays an important role after the squaring stage in cabbage.

3.3. Endogenous Hormones

The relationship between endogenous hormones and bolting has been extensively studied, suggesting that these physiological characteristics are highly associated with bolting in various vegetable crops [59,60]. Early-bolting cultivars maintain higher levels of cytokinin (CTK) and polyamines compared to late-bolting ones in spring Chinese cabbage [61]. Li et al. [59] found that GA content in shoot apical tissues increases in non-heading Chinese cabbage. Bolting in garlic is highly related to methyl jasmonate (MeJA) and endogenous phytohormones, particularly GAs [62]. Han et al. [14] found that chlorophyll, anthocyanin, and auxin levels were lower in a bolting lettuce line. High IAA content in the stem and GA content in the leaves promotes bolting in lettuce [63]. Higher ratios of GA4/ZR (Ribosylzeatin) and IAA/ZR lead to early bolting, whereas a high IAA content and low GA3 content play positive roles in early bolting of carrots [64]. Dai et al. [57] revealed that ABA, ethylene, and chitin-activated signaling pathways are enriched in late-bolting Chinese cabbage.

3.4. Enzyme Activity

Flower bud differentiation is accompanied by changes in enzyme activities in vegetable crops [65], such as SOD (superoxide dismutase) [66] and POD (peroxidase) [65]. Wang et al. [58] found that several indicators are important in bolting after vernalization, such as APX (ascorbate peroxidase) during the squaring stage, MDA after the squaring stage, and G-POD (guaiacol peroxidase) two weeks before the squaring stage in different cabbage genotypes.

3.5. Other Factors

DNA methylation/hypermethylation is critical to vernalization-induced flowering and provides a developmental control mechanism that prevents early flowering [38,59,67]. Yang et al. [68] reported that floral primordium initiation and development is caused by vernalization-induced hypermethylation. He et al. [69] found that partial hyper-acetylation of histones in FLC (FLOWERING LOCUS C) chromatin caused by lesions in FLD (FLOWERING LOCUS D) leads to extremely delayed flowering due to upregulation of FLC expression in the autonomous pathway in Arabidopsis.

4. Molecular Mechanism of Bolting

4.1. Molecular Markers

Researchers have analyzed the association between the flowering time of candidate loci using various molecular markers such as SSR (simple sequence repeat), RAPD(random amplified polymorphic DNA), SCAP (sequence-characterized amplified polymorphism), InDEL (insertiondeletion), AFLP (amplified fragment length polymorphism), SCAR (sequence-characterized amplified regions), SNPs (single-nucleotide polymorphisms) [70,71], CAPS (cleaved amplified polymorphic sequence), and KASP (Kompetitive allele-specific PCR) [72]. They found that one or more flowering-related genes could be candidates in different vegetable crops [9,73], such as cabbage [5,74], Chinese cabbage [75], and radish [76]. VR-DE01 andVR-FT01 were detected on the top of A02 and were closely linked with BrFLC2 in B. rapa [77]. Rosenta et al. [36] identified the environment-specific LsFT gene. Gan et al. [78] constructed a high-density genetic linkage map and detected five genes (Rsa10025681, Rsa10025809, Rsa10025935, Rsa10035523 and Rsa10025740) with sequence variation between parental lines related to flowering and bolting. However, the detailed functions of these candidate genes during bolting and flowering of radish require further research. Some markers have been subjected to marker-assisted selection of flowering time in breeding B. rapa, such as BrFLC1 [79] and BrFLC5 [80]. Wang et al. [81] detected two QTLs in cabbage, located on chromosome C02 at 2.31–3.09 Mb and 33.57–34.40 Mb, respectively, with a total length of 1.61 Mb. In the study by Meng et al. [82], a major qBT1.1, was mapped on chromosome 1 in spinach and narrowed down to 0.56 Mb using KASP markers. Within this region, SpCOL14 (CONSTANS-LIKE), a candidate gene for bolting, has multiple variations in the promoter.

4.2. Mining and Expression of Regulatory Genes

Many researchers have studied the molecular basis of vernalization and discovered that many genes, such as CO (CONSTANS) [9], FLD [69], FLF (FLOWERING LOCUS F) [83], FLC [84,85], FRI (FRIGIDA) [86], and VRN (vernalization) [87,88], regulate plant flowering [89,90,91,92]. Other genes related to bolting resistance have been gradually discovered and mined with the deepening of research on various vegetable crops (Table 1). Gu et al. [93] showed that the effects of the genome on bolting and budding were more than those from BrFLCs, while the background of the cabbage genome influenced the additional cabbage chromosome 4 on BrFLC expression. Han et al. [14] found that 12 flowering-promoting MADS-box genes were specifically induced in bolting-sensitive lines through GA treatment, suggesting that the MADS-box genes are responsible for bolting regulation in lettuce. Large families of regulators that comprise MADS-domain-containing transcription factors play diverse roles in plant development, including regulating flowering time (Figure 1b). The expression of genes decreases/increases upon cold exposure, causing floral induction, which inhibits/promotes bolting and flowering. FLC is a key vernalization response gene but also a floral repressor. DELLA proteins negatively regulate the GA signaling pathway. H4 a cetylation (a common regulator) connects drought and flowering regulation. SVP encodes an MADS-box gene family of transcription factors that repress floral transition. The AP2/ERF (APETALA2/ethylene-responsive element binding factors) gene super family demonstrates potential roles in plant flower development regulation and flower tissue formation [94,95,96].

4.3. Protein and Protein Interaction Regulation

Interactions between proteins such as SVP, FLC, SOC, and AGL are crucial in flowering regulation. In B. juncea, specific amino acid sites regulate these interactions. For example, HDA9 regulates flowering signal integrators SOC1 and AGL24, while DELLA proteins interact with BcGID1b, affecting GA signal transduction in Chinese cabbage. Heat shock proteins and calmodulin interactions under high temperatures also influence GA levels and bolting in lettuce.

5. Genome and Transcriptome Analysis

5.1. Genome and Transcriptome

Genome-wide and transcriptome analyses have identified numerous genes related to bolting and flowering across various crops. For example, radish transcriptome profiling revealed genes involved in vernalization, and candidate genes for bolting in Chinese cabbage have been isolated. DNA methylation and miRNAs play roles in controlling gene expression during bolting, as seen in high-temperature-induced bolting in lettuce.

5.2. RNA (miRNAs/lncRNAs/circRNAs/ceRNA)

miRNAs, lncRNAs, and circRNAs are involved in the regulation of flowering time and bolting. For instance, differential expression of transcription factors in lettuce and miRNA-DEG pairs in radish are significant. ceRNA networks reveal interactions between various RNA molecules and vernalization-related genes, indicating complex regulatory mechanisms.

5.3. Functional Verification and Genetic Transformation

Functional studies of genes like BrFLC1 and BrFLC3 in Brassica crops have shown delayed bolting times in transgenic plants. Such studies enhance the understanding of bolting mechanisms and contribute to breeding strategies for improved bolting resistance.

6. Identification of Bolting and Breeding

6.1. Investigating Epigenetics

Epigenetic modifications such as DNA methylation and histone modifications regulate gene transcription related to bolting and adaptation to environmental stresses. These modifications play a role in vernalization and flowering in Brassica vegetables [120,121,122].

6.2. Identification of the Bolting Properties

To identify bolting properties, methods like principal component analysis (PCA) and subordinate function analysis have been used [68]. These methods evaluate the tolerance to bolting in radish and other crops, helping to select germplasms with desired bolting resistance [123,124]. Zhang et al. [125] divided 64 germplasms into three groups using the membership function method and screened 40 germplasms with moderate bolting tolerance.

6.3. Hereditability and Hereditary Effects

Bolting traits in crops are influenced by major genes and polygenes, with significant environmental variance. Genetic analyses reveal additive–dominant–epistatic effects in crops like Chinese cabbage and cabbage, aiding in the selection of bolting tolerance in early generations [105,126,127,128]. Two major genes expressed in the mode of additive–dominant–epistatic (D-2) effects mainly controlled the bolting trait, and the additive effects of the two major genes were similar in Chinese cabbage [105,126,127,128], cabbage [51,129], pakchoi [130], and carrot [16,20]. However, the environmental variance was high in total variance, so selecting for bolting tolerance was in its early stages [130]. The average heritability of major genes and polygenes was 93.41% in cabbage [51]. Ji et al., [127] indicated that in B. rapa, one or two major genes controlled the bolting trait. Genetic analysis revealed that in Chinese cabbage, an incomplete dominant gene BrLb-1 controlled the late-bolting to early-bolting trait [106].

6.4. Breeding Methods

Breeding methods, including crossbreeding and mutation breeding, are essential for developing new plant species and varieties that meet specific needs, such as delayed bolting.
Crossbreeding: Gu et al. [94] obtained cabbage plants with different chromosome counts (2n = 21 and 2n = 20) through cross combinations. Plants with 2n = 21 chromosomes bolted later than those with 2n = 20 from the same hybridized combination. Motoki et al. [131] explored whether transmissible agents from rootstocks could induce flowering in cabbage without low-temperature treatment. They concluded that the pathway to vernalization in these plants is independent of cabbage BoFT and BoFT expression from the scion.
Mutation breeding: Ipek et al. [132] discovered a 1403 bp mitochondrial DNA marker associated with bolting in garlic, speculating that it resulted from an insertion mutation during garlic’s evolution. Li et al. [133] developed a new cultivar of non-heading Chinese cabbage named Yanchun using space mutation combined with traditional breeding methods. Wang et al. [114] identified an RsFLC2 gene with a 1627 bp insertion near its first intron, linked to latebolting in radish. Liu et al. [124] demonstrated that a 1628 bp insertion in the FLC2 gene’s first intron in radish significantly impacted late bolting, with homozygous mutations having a more pronounced effect than heterozygous ones. Abuyusuf et al. [134] used the InDel method to design molecular markers (BolPrx.2) to characterize bolting time variations in cabbage, predicting about 84% of the variation within commercial and population lines. Fu et al. [135] found an early-bolting mutant in Chinese cabbage caused by a single-nucleotide C-to-T substitution in the BrFLC2 gene, controlled by a recessive nuclear gene. Li et al. [136] identified a 215 bp deletion in the BoFLC2 gene intron I, which slowed its silencing activity, leading to late flowering in cabbage. Tang et al. [137] noted that the 9325 bp loss of the BoFLC gene caused a non-vernalization requirement, leading to the development of its codominant marker for breeding B. oleracea crops.
Gene editing: Shin et al. [138] used CRISPR/Cas9 to edit AGL19 and AGL24 genes in Chinese cabbage, resulting in late-bolting T-DNA free lines. Shin and Park [139] edited the BrLEAFY (BrLFY) gene using CRISPR/Cas9, producing T-DNA-free E1 LFY-edited lines that showed continuous vegetative growth and late bolting. Choi et al. [140] conducted CRISPR/Cas9-mediated single-base mutation in the SOC1 gene of lettuce, delaying the formation of the first flower bud and lowering the expression of several floral regulatory genes (LsFUL, LsAPL1, LsAPL2, and LsLFY).

7. Discussion

7.1. Studying Blooming in Other Crops

Research on bolting and blooming spans various crops, highlighting the importance of shoot apical meristem transitions to inflorescence and floral meristems. This process is crucial for seed production but can negatively affect the plant’s medicinal, market, and economic value. Studies have been conducted on medicinal plants (e.g., Angelica sinensis) [141], oil crops (B. rapa) [142], commercial crops (sugar beet) [143], grain crops (barley, rice, wheat) [144,145,146], flower crops (Agave thaliana, Dendrobium nobile, Lilium longiflorum, and Aquilegia coerulea) [147,148,149,150], and forage crops (Medicago truncatula, orchard grass) [94,151]. Shojaei et al. [152] identified COP1 and CDF in the photoperiod pathways of sugar beet. Kane et al. [153] found that TaVRN1 transcription in wheat was repressed by TaVRT2. Takada et al. [154] indicated that BrFRIb functions as an activator of BrFLC in B. rapa, showing that H3K27me3 accumulation represses BrFLCs. Liang et al. [155] uncovered differentially expressed lncRNAs and mRNAs in B. vulgaris, revealing candidate vernalization genes encoding B3-domain-containing proteins.

7.2. Advantages and Disadvantages of Early and Late Bolting

Understanding the molecular mechanism of vernalization is crucial for breeding high bolting resistance. Preferences for early or late bolting depend on market needs.
Early bolting: Suitable for quality seed production, but may damage the economic potential of leafy, fleshy root, and succulent stem vegetable crops.
Late bolting: Increases market value by allowing more extensive vegetative growth and is ideal for leafy, root, and stem crops. Bolting time is often linked to leaf senescence (LS). Early LS is associated with early bolting, while late LS is associated with late bolting. The A. trithorax (ATX) enzymes, for instance, regulate transitions between vegetative and reproductive phases: Hinckley and Brusslan [156] generated an atx1, atx3, and atx4 triple-T-DNA-insertion mutant showing both early LS and early bolting in Arabidopsis. Dai et al. [57] revealed that leaf senescence is related to bolting and flowering in Chinese cabbage, with several hub genes (e.g., CPRD49, AAP8, MTHFR2, BXLs, WRKYs, GATLs) regulating vernalization.

8. The Concluding Overview

Research on bolting and flowering in vegetables has gained traction, with notable studies on plants like water dropwort, flowering Chinese cabbage, watercress, and Brasenia schreberi. There is a need to balance the cultivation of bolting-resistant vegetables with market demand for characteristic vegetables that bolt easily.
Despite advancements in controlling bolting through improved facility conditions, open-field cultivation still faces significant challenges, particularly in developing regions like southwestern China. Future research should focus on genomics, molecular markers, and gene editing techniques to develop early- or late-bolting varieties tailored to the vegetable industry’s needs.

Author Contributions

G.-F.T., Q.L., Z.-F.C. and A.-S.X. conceived the paper; G.-F.T. wrote the manuscript; G.-F.T., S.-H.Z., X.-L.Z., P.-H.M. and M.-Y.L. collected and cultured the plant material; Q.L. and G.-F.T. conducted analysis; Q.L., Z.-F.C., A.-S.X. and G.-F.T. contributed substantially to revisions. All authors commented on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by The Construction of Biological Breeding Platform for Important Crops in Karst Mountain Areas of Cuizhou Province (Qian Ke He Zhong Yin Di [2023]033); Project of Guizhou Provincial Department of Science and Technology (Qiankehe Foundation-ZK [2024] General 543; Qiankehe Fuqi No. [2022] 005; Guizhou Provincial Key Technology R&D Program ([2021] No. 207); Project of Guizhou Academy of Agricultural Sciences (Science and Technology Innovation of Qiannongkeyuan No. [2022] 07); Jiangsu Seed Industry Revitalization Project (JBGS(2021)068).

Conflicts of Interest

The authors declare no conflicts of interest.

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Horticulturae 10 00670 g001
Figure 1. Regulatory mechanism of bolting traits in different vegetable crops. (a) Preconditions in bolting of various vegetable crops. (i): celery; (ii): cabbage; (iii): radish; (iv): choy sum; (v): red liverwort; (vi): lettuce; (vii): carrot; (viii): cauliflower; (ix): Chinese cabbage; (x): mustard; (xi): liverwort; (xii): asparagus lettuce; (xiii): garlic; (xiv): scallion; (xv): spinach; (xvi): turnip; (xvii): pakchoi; (xviii): garland chrysanthemum; (b) Regulatory genes. (i): promoting regulatory factors; (ii): inhibiting regulator factors. Gray frame: crops of different families; black dotted line: different vernalization; yellow frame: floral integrator that promotes flowering; green frame: gene editing; red frame: positive regulation factors; blue frame: negative regulation factors; →: positive interaction; red arrows: increase or decrease of expression; ▬|: negative interaction. ATX: Arabidopsis trithorax; LS: leaf senescence; IAA: indoleacetic acid; ARF: auxin response factor; CO: CONSTANS; SOC1: suppressor of overexpression ofconstans 1; LFY: leafy; GA: gibberellin; MeJA: methyl jasmonate; VIN1: vernalization insensitive 1; lncRNA: long noncoding RNA; VAS: VRN1 alter native splicing; VRNI: VERNALIZAITON1; VRG: vernalization-related gene; ABA: abscisic acid; CDF: cycling dof factor; COP1; constitutive photomorphogenesis 1; FLD: FLOWERIG LOCUS D; FLC: FLOWERIG LOCUS C; FT: flowering locus T; Ft: floweringtime; VRT2: vegetative to reproductive transition 2; SVP: short vegetative phase; ZCE1: cis-CA (zusammen-CA)-enhanced 1; FK: FACKELl; VRN2: vernalization 2; COL14: CONSTANS-like 14; TFs: transcription factors; VIL: VIN3-like (VIN3: vernalization-insensitive 3); Brebm: early-bolting mutant in Chenese cabbage; FRIb: FRIGIDAb; miR396: microRNA396; HSP: heat shock protein; FTal: FT orthologue; RGL1: RGA-LIKE1; GA3ox: GA3-oxidase.
Figure 1. Regulatory mechanism of bolting traits in different vegetable crops. (a) Preconditions in bolting of various vegetable crops. (i): celery; (ii): cabbage; (iii): radish; (iv): choy sum; (v): red liverwort; (vi): lettuce; (vii): carrot; (viii): cauliflower; (ix): Chinese cabbage; (x): mustard; (xi): liverwort; (xii): asparagus lettuce; (xiii): garlic; (xiv): scallion; (xv): spinach; (xvi): turnip; (xvii): pakchoi; (xviii): garland chrysanthemum; (b) Regulatory genes. (i): promoting regulatory factors; (ii): inhibiting regulator factors. Gray frame: crops of different families; black dotted line: different vernalization; yellow frame: floral integrator that promotes flowering; green frame: gene editing; red frame: positive regulation factors; blue frame: negative regulation factors; →: positive interaction; red arrows: increase or decrease of expression; ▬|: negative interaction. ATX: Arabidopsis trithorax; LS: leaf senescence; IAA: indoleacetic acid; ARF: auxin response factor; CO: CONSTANS; SOC1: suppressor of overexpression ofconstans 1; LFY: leafy; GA: gibberellin; MeJA: methyl jasmonate; VIN1: vernalization insensitive 1; lncRNA: long noncoding RNA; VAS: VRN1 alter native splicing; VRNI: VERNALIZAITON1; VRG: vernalization-related gene; ABA: abscisic acid; CDF: cycling dof factor; COP1; constitutive photomorphogenesis 1; FLD: FLOWERIG LOCUS D; FLC: FLOWERIG LOCUS C; FT: flowering locus T; Ft: floweringtime; VRT2: vegetative to reproductive transition 2; SVP: short vegetative phase; ZCE1: cis-CA (zusammen-CA)-enhanced 1; FK: FACKELl; VRN2: vernalization 2; COL14: CONSTANS-like 14; TFs: transcription factors; VIL: VIN3-like (VIN3: vernalization-insensitive 3); Brebm: early-bolting mutant in Chenese cabbage; FRIb: FRIGIDAb; miR396: microRNA396; HSP: heat shock protein; FTal: FT orthologue; RGL1: RGA-LIKE1; GA3ox: GA3-oxidase.
Horticulturae 10 00670 g001
Table 1. Expression and functional characteristics of gene and regulatory factors.
Table 1. Expression and functional characteristics of gene and regulatory factors.
FamiliesSpeciesGene Characteristic of Genes, Expression, and RegulationReferences
BrassicaceaeCabbage (B. oleracea L.)BoFLC2Negative regulation[97,98]
BoVIN3Stems; gene length was 1680 bp; amino acid was 560 aa; isoelectric point was 6.56[99]
BoFLC(1,2,3)Conserved with the MADS-box domain[42]
AGL18, HDA9Gene length was 777 and 1281 bp, conserved region was MIKC/HDAC; amino acids were 258 and 426 aa; negative regulation[100]
AGL19, SOC1, AGL24Amino acids were 221, 221, and 214 bp, conserved region was MIKC; AGL19 and SOC1 were SOC1/TM3 subfamily; positive regulation[101,102]
Chinese cabbage (B. rapa L.)BrFLC5Weak positive regulator[103]
BrFLC2A candidate gene for a vernalization[99]
BrFLC, BrMAF, BrVIP, BrVRNNegative regulation, response to vernalization; BrVRN and BrVIP genes showed different expression patterns[33]
BrHIS4.A04A histone H4 gene; prevents premature bolting by weakening the expression of flowering genes under drought conditions through the ABA signaling pathway[104]
BrEb-1Positive regulation; an incomplete dominant gene, mapped from 20,070,000 to 25,290,000 bp (5.22 Mb) and harbored on chromosome A07[105]
BrPIF4, BrPIF5, BrFLCs, BrFRL, BrMAF1s, BrCOLsBrPIF4, BrPIF5, and BrCOLs were predominantly expressed in core tissues, promoting bolting, BrFLCs, BrFRL, and BrMAF1s were predominantly expressed in core tissue[106]
BrSVPNegative regulation; repressed the expression of the floral integrator genes AGL20, AGL24, and FT during vernalization[107]
B. rapa ssp. pekinensisBrpFLCNegative regulation; gene length was 851 bp and contained a 591 bp ORF; amino acid length was 197 aa; conserved region was MADS-box; belongs to a multi-gene family[108]
B. campestris ssp. chinensisBcFLC-1, BcFLC-2, BcFLC3Negative regulation, responded to low-temperature vernalization in leaves; gene length was 1017 bp; conserved region was MADS-box; amino acid length was 197 aa; isoelectric point was 9.36; multi-copy[109,110]
Chinese cabbageBcSOC1Positive regulation; promoted stem elongation and bolting in flowering Chinese cabbage[51]
DELLANegative regulation of GA signal transduction; its proteins contained VHYNP-, DELLA-, SAW-, and VHIID-conserved domains; tissue-specific expression[111]
Radish (R. Sativus L.)BrcuFRI, BrcuFLCBrcuFRI in stems and leaves, while BrcuFLC in roots; Gen Bank accession number was EU700362/EF138603[86]
RsFLC, RsSOC1RsFLC was Ft genes; negative regulation;RsSOC1 positive negative[112]
RsFLC2A late-bolting gene was detected in a 1.1 cM on chromosome R02; contains a 1627 bp insertion; weakened gene repression[113]
FLC1.1, FLC1.2, VRN1, VRN2, SOC1FLC1.1 and FLC1.2 induced positive regulation while VRN1, VRN2, and SOC1 induced negative regulation[54]
Carrot (D. carota L.)DcFLC1, DcFLC2, DcFLC3DcFLC1 and DcFLC3 responded to low temperature in late bolting while DcFLC2 responded to light; amino acid length was 209, 212, and 219 aa; conserved region was MADS-box/K-box[114]
Vrn1, Rf1Early-flowering gene, mapped to chromosomes 2 and 9 with flanking markers from 0.70 to 4.38 cM and 0.46 to 1.12 cM[115]
DcSOC1-1DcSOC1-2DcSOC1-1 promoted by long day early-bolting; amino acids were 217 and 211 aa, conserved region was MADS-box/K-box, sub cellular location was SOC1/TM3 subfamily[116]
Lettuce (L. sativa L.)LsARF3Response to high temperature; activate the expression of LsCO[117]
LsARF8a24 LsARFs in the lettuce genome; have been classified into three clusters; respond to heat[118]
LsRGL1One of the DELLA-encoding genes; negatively regulates the GA pathway; interacts with LsGA3ox and the LsYUC4 promoter region[50]
LsFTOver expression of it recovered the late-flowering phenotype of ft-2 mutant and it was promoted by heat treatment; knockdown of it by RNA interference dramatically delayed bolting[119]
FLC: FLOWERIG LOCUS C; VIN: vernalization insensitive; AGL: agamous-like; HAD 9: histone deacetylase 9; SOC1: suppressor of overexpression on constans 1; MAF1: MADS AFFECTING FLOWERING1; VIP: VERNALIZA TION INDEPENDENCE; VRN: VERNALIZAITON; PIF: PHYTOCHROME-INTERACTINGFACTOR; FRL: FRIGIDA-LIKE; SVP: short vegetative phase; FRI: FRIGIDA; COL1: CONSTANS-like 1; CLF: curly leaf; VRT-2: vegetative transition gene 2; ARF: auxin response factor; RGL1: RGA-LIKE1; FT: FLOWERING LOCUS T.
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Tan, G.-F.; Luo, Q.; Zhu, S.-H.; Zhong, X.-L.; Meng, P.-H.; Li, M.-Y.; Chen, Z.-F.; Xiong, A.-S. Advancements in Molecular Mechanism Research on Bolting Traits in Vegetable Crops. Horticulturae 2024, 10, 670. https://doi.org/10.3390/horticulturae10070670

AMA Style

Tan G-F, Luo Q, Zhu S-H, Zhong X-L, Meng P-H, Li M-Y, Chen Z-F, Xiong A-S. Advancements in Molecular Mechanism Research on Bolting Traits in Vegetable Crops. Horticulturae. 2024; 10(7):670. https://doi.org/10.3390/horticulturae10070670

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Tan, Guo-Fei, Qing Luo, Shun-Hua Zhu, Xiu-Lai Zhong, Ping-Hong Meng, Meng-Yao Li, Zhi-Feng Chen, and Ai-Sheng Xiong. 2024. "Advancements in Molecular Mechanism Research on Bolting Traits in Vegetable Crops" Horticulturae 10, no. 7: 670. https://doi.org/10.3390/horticulturae10070670

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