Next Article in Journal
S-Series Coelenterazine-Driven Combinatorial Bioluminescence Imaging Systems for Mammalian Cells
Next Article in Special Issue
Biology of Two-Spotted Spider Mite (Tetranychus urticae): Ultrastructure, Photosynthesis, Guanine Transcriptomics, Carotenoids and Chlorophylls Metabolism, and Decoyinine as a Potential Acaricide
Previous Article in Journal
Cellular and Molecular Biology of Cancer Stem Cells of Hepatocellular Carcinoma
Previous Article in Special Issue
Accumulation of Anthocyanins in Detached Leaves of Kalanchoë blossfeldiana: Relevance to the Effect of Methyl Jasmonate on This Process
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 24
Issue 2
10.3390/ijms24021419
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Basic Helix-Loop-Helix Transcription Factors: Regulators for Plant Growth Development and Abiotic Stress Responses

by
Zhi-Fang Zuo
†,
Hyo-Yeon Lee
and
Hong-Gyu Kang
*
Subtropical Horticulture Research Institute, Jeju National University, Jeju 63243, Republic of Korea
*
Author to whom correspondence should be addressed.
†
Current address: Key Laboratory of National Forestry and Grassland Administration on Grassland Resources and Ecology in the Yellow River Delta, College of Grassland Science, Qingdao Agricultural University, Qingdao 266109, China.
Int. J. Mol. Sci. 2023, 24(2), 1419; https://doi.org/10.3390/ijms24021419
Submission received: 28 November 2022 / Revised: 30 December 2022 / Accepted: 4 January 2023 / Published: 11 January 2023
(This article belongs to the Collection Feature Papers in Molecular Plant Sciences)
Browse Figures
Review Reports Versions Notes

Abstract

:
Plant basic helix-loop-helix (bHLH) transcription factors are involved in many physiological processes, and they play important roles in the abiotic stress responses. The literature related to genome sequences has increased, with genome-wide studies on the bHLH transcription factors in plants. Researchers have detailed the functionally characterized bHLH transcription factors from different aspects in the model plant Arabidopsis thaliana, such as iron homeostasis and abiotic stresses; however, other important economic crops, such as rice, have not been summarized and highlighted. The bHLH members in the same subfamily have similar functions; therefore, unraveling their regulatory mechanisms will help us to identify and understand the roles of some of the unknown bHLH transcription factors in the same subfamily. In this review, we summarize the available knowledge on functionally characterized bHLH transcription factors according to four categories: plant growth and development; metabolism synthesis; plant signaling, and abiotic stress responses. We also highlight the roles of the bHLH transcription factors in some economic crops, especially in rice, and discuss future research directions for possible genetic applications in crop breeding.

1. Introduction

In all eukaryotic organisms, transcription factors regulate many biological processes by controlling the expressions of downstream target genes. Transcription factors can be grouped into different subfamilies according to their DNA-binding domains [1]. Basic helix-loop-helix (bHLH) transcription factors are among the superfamilies that are commonly found in plants and animals [2]. The conserved bHLH domain contains approximately 60 amino acids (aa), including a basic DNA binding region and two amphipathic α-helices that are separated by a loop region with a variable length [3]. The basic region consists of the first 15 amino acids. Most bHLH proteins have a glutamic acid residue at position 9 (E9), which can interact with the CA nucleotides in the DNA sequence [4,5]. Around 15 base-pair α-helices region in the C-terminus contain several hydrophobic amino acids, such as isoleucine (I), leucine (L), and valine (V), which promote the formation of dimeric complexes [5]. In addition, the variable loop region found in the middle of two α-helices is involved in the formation of the homodimers or heterodimers between bHLH proteins [5].
Metazoans are classified into six distinct phylogenetic groups (A–F) based on expression patterns, dimerization selectivity, and DNA-binding specificities of the bHLH domains [6]. Group A proteins bind the CAGCTG E-box configuration to form homodimers or heterodimers, such as E12, E47, and Daughterless (Da). Group B proteins bind the CACGTG E-box configuration to play important role in various developmental and cellular processes. Group C proteins contain the PAS domain that bind the ACGTG or GCGTG core sequences, which control the development of neurogenesis and the midline, as well as the formation of the tracheal and salivary ducts. Group D proteins are unable to bind DNA due to the absence of the basic domain that neutralizes the DNA-binding activities through heterodimerization. Group E proteins recognize typical sequences in the N box (CACGCG or CACGAG) that contain another two characteristic domains (‘Orange’ domain and WRPW peptide) in their C-terminus. Group F proteins contain a highly conserved COE domain that is involved in dimerization and DNA binding [7,8].
In plants, scientists have classified the bHLH transcription factors based on their characteristics. Pires and Dolan [4] studied the evolution of the bHLH transcription factors from land plants to algae, and they classified 544 bHLH transcription factors into 26 subfamilies. A total of 20 subfamilies shares the same ancestors as extant moss and vascular plants, while 6 subfamilies exist in vascular plants. In addition, Carretero-Paulet [9] present an updated and comprehensive classification of the bHLH transcription factors that extend the subgroup to 32 in plants using 638 bHLH genes. The plant bHLH transcription factors regulate many growth and development processes, such as embryo growth (Retarded Growth of Embryo1, RGE1), development of the reproductive organs including gynoecium (HECATEs, HECs) and anthers (Dysfunctional Tapetum1, DYT1), fruit dehiscence (INDEHISCENT, IND), and seed dispersal (ALCATRAZ, ALC) [10,11,12,13,14]. Furthermore, bHLH proteins also function in metabolism biosynthesis and signal transduction, such as in anthocyanin synthesis (Transparent Testa8, TT8), light signaling (Phytochrome Interacting Factors, PIFs), and brassinosteroid signaling (BEEs) [15,16,17]. Moreover, some bHLH subfamily members play important roles in plant biotic and abiotic stress responses, such as pathogen Xanthomonas albilineans (SsbHLH15/17), cold (Inducer of CBF Expression1/2, ICE1/2), and salt stress (SlbHLH) [18,19,20,21].
Due to the progressive evolution of sequencing technologies, many genome databases are available for many important plants. Recently, many researchers have performed genome-wide studies on bHLH transcription factors in various crops, and they have widely studied the functions of bHLH transcription factors in the model plant Arabidopsis thaliana; however, we lack extensive studies on the functions of the bHLH transcription factors in other plants. In this review, we first classify the information on the functionally characterized bHLH transcription factors according to four categories: (i) plant growth and development; (ii) metabolism synthesis; (iii) plant signaling, and (iv) abiotic stress response, and we explore their roles in various crops, and especially in rice. We also discuss the research gap and perspectives for future research for the genetic applications of bHLH transcription factors in crop breeding.

2. The bHLH Transcription Factor Family in Plants

Researchers first identified genome-wide bHLH genes in plants from Arabidopsis (147) and rice (167), and it has become one of the largest transcription factor families in their host plants [22,23]. Nowadays, researchers have widely identified bHLH gene families in various species, and they have grouped them into different numbers of subfamilies, which we present in Figure 1 (Figure 1). The bHLH protein evolutionary relationship between different species suggest that most of these subfamilies are derived from the same ancestors, and may play a fundamental role during the plant development and evolution. The functional losses of some subfamily proteins during plant evolution may have led to decreases in their evolutionary branches. In this review, we divide the bHLH transcription factors into 16 subfamilies, which we present in Table 1. Researchers have extensively studied bHLH subfamily III, which includes III(a+c), III(b), III(d+e), and IIIf; however, the bHLH genes in subfamilies V, VIIIb, and XI have rarely been identified, which indicates the tendency towards the bHLH transcription factors in plants.

2.1. bHLH Transcription Factors Are Responsible for Plant Growth and Development

bHLH transcription factors regulate plant growth and development. Researchers have demonstrated bHLH gene functions in Arabidopsis, as summarized by Hao et al. [65]. However, few bHLH genes have been characterized in other crop plants. Here, we focus on the functionally characterized bHLH genes in different plants, and mainly in crops (Figure 2).
The members of the same subfamily always have similar functions. In flowering plants, the anther is a reproductive organ that is composed of meiocytes and four cell layers: the epidermis, endothecium, middle layer, and tapetum [66]. The rice bHLH transcription factor in subfamily II, TDR Interacting Protein 2 (TIP2), plays an important role in the formation of the middle layer and tapetum during early anther development through the regulation of Tapetum Degeneration Retardation (TDR) and Eternal Tapetum 1 (EAT1). TDR and EAT1 are the key regulators in rice tapetal programmed cell death [67]. EAT1, which is a conserved bHLH transcription factor in land plants, is involved in this complex process via the direct activation of the transcriptions of two aspartic protease encoding genes (AP25 and AP37) [68]. In addition, EAT1 also regulate meiotic phasiRNA biogenesis in anther tapetum, and Undeveloped Tapetum 1(UDT1) is a potential interacting partner of both EAT1 and TIP2 during the early meiosis process in rice [69,70]. Furthermore, rice TIP2 and EAT1 belong to subfamily II, which indicate that the bHLH genes in subfamily II may act as the key transcriptional regulators in anther development (Table 1). The overexpression of OsbHLH35 endows plants with small and curved anthers, which result in a reduction in the seed production (Figure 2) [71]. In this process, three Growth Regulating Factor (GRF) family members, including OsGRF3, OsGRF4, and OsGRF11, act as the transcriptional regulators of OsbHLH35, and OsGRF11 acts as a negative regulator of OsbHLH35 in rice. In other plants, LoUDT1 from the oriental lily hybrid Siberia (Lilium spp.), which is the homologous gene of OsUDT1, is also related to anther development [72]. Citrullus lanatus Abnormal Tapetum 1 (ClATM1), which is the first male sterility gene in watermelon, encodes a bHLH protein, and plays important role in the regulation of anther development, which researchers verified via CRISPR/Cas9-mediated mutagenesis [73]. In tomato, Solyc01g081100, which is a homolog of OsEAT1, is the candidate gene for the dysfunctional pollen and tapetum development in the male sterile 32 (ms32) mutant, and the CRISPR/Cas9-mediated modification of the bHLH protein encoded gene Solyc02g079810 causes male sterility in tomato plants [74,75].
The antagonist of the PGL1 (APG) of rice in subfamily VII(a+b), called OsPIL16, controls the grain length and weight [76]. OsPIL16 interacts with two atypical bHLH transcription factors, Regulator of Grain Length 1 (PGL1) and PGL2, to antagonistically regulate the development of the rice grain length [76,77]. The overexpression of PGL1 in lemma/palea increased the grain length and weight in transgenic rice [77]. In addition, OsPIL15 shares a close genetic relationship with OsPIL16, which also influences cell division by affecting the transport of cytokinin (CTK), which results in decreased cell numbers in rice grains [78]. Yang et al. [79] demonstrated that OsbHLH107, which is in the same subfamily as the OsPIL genes, also participates in the regulation of grain size. In another important crop plant, maize, transcription factor ZmbHLH121 in subfamily VIIIb positively regulates the kernel size and weight of maize [80].
Root hairs are long tubular projections of trichoblasts, which are the hair-forming cells on the epidermis of the plant root. They increase the plant surface area to improve absorption of nutrients from soil [81,82]. The rhizoid root hairs are essential for ion exchange, anchorage functions, and microbial interactions in the soil of land plants [81]. Various bHLH transcription factors participate in this critical root development process [83]. During root hair cell differentiation, the hair and non-hair cells are differentiated from morphologically identical epidermal cells [84]. The root hair cells produce an outside long tubule from the hair-forming cells on the epidermis of the plant root, and they function in the absorption of nutrients and water, and in interaction with microbes [82,83]. In
Arabidopsis root hair defective 6 (Atrhd6) and root hair defective six-like1 (Atrsl1) double mutants that lack the RSL class I gene function, transformation with 35S: OsRSL1, 35S:OsRSL2 or 35S:OsRSL3 restored the expressions of the RSL class II genes, which indicates the functional conservation of the RSL genes between rice and Arabidopsis in root hair development [85]. In Brachypodium distachyon, the RSL class I genes, including BdRSL1, BdRSL2, and BdRSL3 also promote root hair development [86]. In sweet sorghum, researchers identified a new atypical bHLH transcription factor, SbbHLH85, in subfamily VIIIc(2), as a key gene for root development via increase in the numbers and lengths of the root hair via ABA and auxin signaling pathways [87].

2.2. bHLH Transcription Factors Play Important Roles in Plant Metabolism Synthesis

Anthocyanins are the major pigments of flavonoid compounds, and they endow plants with colors, such as blue, purple, and red, in many flowers, fruits, and vegetables [88,89]. In plants, anthocyanins attract pollinators or seed dispersers, and they protect against UV radiation, pathogen attacks, and abiotic stresses [90,91]. Furthermore, anthocyanins are compounds with potential health-benefits for lowering the risk of cardiovascular diseases, certain cancers, and diabetes in humans due to high levels of antioxidant activity [92,93,94]. The MBW complex (R2R3-MYB, bHLH, and WDR) mediates the anthocyanin biosynthetic pathway, which is one of the most conserved and well-studied secondary metabolism pathways in plants [95,96].
The functionally regulated bHLH genes in anthocyanin biosynthesis are primarily classified as subfamily IIIf. Petroni and Tonelli [90] and Jaakola [97] reviewed the bHLH genes that are involved in anthocyanin biosynthesis in various horticultural species, such as petunia, antirrhinum, and grape (Table 1). In rice, Sun et al. [98] explored the minimal MBW members required for anthocyanin biosynthesis, including S1 (bHLH), C1 (MYB), and WA1 (WD40). Under chromium stress, the rice MBW complex is regulated by the jasmonate (JA) signal and represses anthocyanin accumulation in tissues (Figure 2) [99]. Additionally, low temperature induced SlAH in subfamily IVd regulates anthocyanin biosynthesis in tomatoes to protect young seedlings from cold stress, which indicates the bHLH transcription factor functional connections between anthocyanin biosynthesis and abiotic stress [100]. In Freesia hybrida, subfamily IIIf, the bHLH transcription factors FhTT8L and FhGL3L interact with FhMYB5 in proanthocyanidin biosynthesis during flower pigmentation [101]. Peach PpbHLH3 regulated the anthocyanin biosynthesis with MYB10.1 and MYB10.3 in fruit development during ripening (at the transition from the S3 to S4 stage) [102]. In sweet cherry, PabHLH3 enhances anthocyanin synthesis with PaMYB10.1-3 in fruits. This process is inhibited by PabHLH33, which is another bHLH transcription factor in subfamily IIIf [103]. The bHLH transcription factor AcB2 from onion is associated with anthocyanin accumulation via the interaction with AcMYB1, which acts as an activator in the flavonoid biosynthetic pathway in the epithelial cells of onion bulbs.
In addition, the rice bHLH transcription factor Diterpenoid Phytoalexin Factor (DPF) in subfamily IVd positively regulates the expressions of the diterpenoid phytoalexin (DP) biosynthesis genes in the process of DP accumulation. DPF was the first bHLH transcription factor to be characterized in DP biosynthesis through the N-box (5′-CACGAG-3′) [104]. In an orphan group from tomato, the bHLH transcription factor SlAR plays an important role in the carotenoid biosynthesis in the fruits, which may particularly affect lycopene accumulation [105].

2.3. bHLH Transcription Factors Are Involved in Plant Signaling

Green plants obtain most of their energy from light through photosynthesis, and light is an important environmental factor that determines plant growth and development. Plants can sense the red, far-infrared, and blue light spectra through photoreceptor systems, including phytochromes (PHYs), cryptochromes (CRYs), and phototropins (PHOTs), and they can then mediate the transcriptional networks in the light-regulated processes [106,107,108,109,110]. In Arabidopsis, members of the phytochrome-interacting factors (PIFs) in subfamily VII(a+b), such as PIF1/ PIF-like (PIL5), PIF3, PIF4, PIF5/PIL6, PIF6/PIL2, and PIF7, can interact with PHYs and play central roles in light signaling regulation [65].
Rice has six PILs (OsPIL11 to OsPIL16) in subfamily VII(a+b), and some of the members are involved in the light signaling pathways [109,110,111,112]. OsPIL15 was negatively regulated by light with the onset of light exposure in etiolated seedlings [113]. The overexpression of OsPIL15 produced exhibited shorter above-ground parts, an undeveloped root system, smaller tiller angles, and enhanced shoot gravitropism, which were related to the skotomorphogenesis development, which was likely regulated by the auxin [114,115]. In addition, Li et al. [116] demonstrated that the fusion of the SRDX transcriptional repressor motif in the C-terminal of OsPIL11 and OsPIL16 caused constitutively photomorphogenic phenotypes with short coleoptiles and open leaf blades in darkness. Nevertheless, OsPIL16 was able to bind to the N-box region of the OsDREB1B promoter, and it was substantially induced by cold stress in a phyB mutant [117]. In peach, PpPIF8 can interact with PpDELLA2 through an unknown motif, and the overexpression of PpPIF8 in Arabidopsis promoted increases in the plant height and branch numbers [118]. Taken together, cross talk may exist among the grain development, light signaling and abiotic stress response that are meditated by PIL or PIF genes. These processes that connect the signal transfer to the molecular gene expression indicate the biochemical mechanisms of photomorphogenesis in plants (Figure 2).
Phytohormones, such as JA and abscisic acid (ABA), regulate plant growth, development, and defense processes. JA triggers the degradation of the protein jasmonate ZIM-domain (JAZ) by 26S protease, which induces the activation of multiple downstream JA-mediated responsive genes [119,120,121,122]. Some bHLH transcription factors are involved in the hormone signaling pathways in plants. RERJ1, which is a rice JA-responsive gene in subfamily III(a+c), was up-regulated via exposure to wounding or drought stress [123]. Interestingly, RERJ1 also interacted with OsMYC2 to mediate the defense processes against herbivory and bacterial infection through JA signaling [124]. The DPF in rice was also induced by JA, and as well as response to blast fungus infection, copper chloride, and UV light [104]. Additionally, JA-regulated OsMYC2 induced the expressions of insect defense-related genes, and it simultaneously activated some of the biosynthetic pathways for the defense-related metabolites in rice, which was proven in a knockdown osmyc2RNAi plant (Figure 2) [124]. In Artemisia annua, AaMYC2-Like, the methyl jasmonate (MeJA) responsive transcription factor, played a prominent role in regulating the artemisinin biosynthetic pathway, as researchers confirmed through the transient overexpression of AaMYC2-Like in the leaves [125]. Furthermore, two MYC-type bHLH transcription factors from A. annua, AabHLH2 and AabHLH3 act as transcription repressors and functional redundantly to regulate artemisinin biosynthesis [126]. ABA plays a central role in a variety of physiological processes, and it is also a key abiotic stress-related hormone that responds to various environmental stresses in plants, such as cold, drought, and salt. Several bHLH transcription factors in subfamily IIIb are involved in abiotic stresses via the ABA signaling pathway. A group of PebHLH genes in moso bamboo (Phyllostachys edulis) possess various cis-elements for ABA and JA in their promoters, which are up-regulated by biotic and abiotic stresses, ABA and MeJA stimuli [31].
Under specific conditions, multiple phytohormones and environmental factors are constantly cross talking to affect plant growth and development. Based on previous studies, light usually promotes cell expansion in plant growth, while ABA and JA are normally involved in the biotic and abiotic stress responses. Some bHLH transcription factors play important roles in signal transduction networks that are mediated by plant hormones. Phytohormones and environment-responsive bHLH transcription factors participate in various plant developmental processes by interacting with each other either cooperatively or antagonistically to modulate plant growth.

2.4. bHLH Transcription Factors Are Related to Plant Abiotic Stress and Iron Homeostasis

Plants have evolved to adapt to the stressful conditions that are unfavorable for their growth and development [127,128,129,130]. However, these adverse environmental conditions substantially affect the yields of crops such as rice [131,132,133]. Cold stress impacts plant productivity, especially during the flowering stage, which substantially lowers the probability of reproductive success. Cold stress signals can be perceived by putative sensors and induce the expressions of stress-responsive genes to modulate the cellular activities through the cytosolic Ca2+ levels [133]. bHLH genes that are related to plant abiotic stresses are mainly in subfamily IIIb, including OsICE1 and OsICE2, which researchers have widely identified in recent years (Table 1).
In rice, OsbHLH148 responds to the initial JA signal and regulates drought responsive genes, including OsDREBs and OsJAZs, endowing the rice with drought tolerance [134]. BEAR1, which is a bHLH gene, regulates the salt response, which was demonstrated by the salt-sensitive phenotypes of its knockdown or knockout transgenic rice [135]. The osbhlh024 mutant (A91), with a nucleotide base deletion generated by the CRISPR/Cas9 strategy, increased the shoot weight, and produced high antioxidant activities under salt stress, which indicates that OsbHLH024 might play a negative role in the salt stress response of rice [136]. In addition, OsWIH2, which is a drought induced WIH gene, was activated by OsbHLH130, and the overexpression of OsbHLH130 resulted in substantially higher drought tolerance via its participation in cuticular wax biosynthesis, with reductions in the water loss rate and ROS accumulation (Figure 2) [137]. OsbHLH057 targeted the AATCA cis-element, in the promoter of Os2H16, a gene responding to fungal attack in rice, and overexpression of OsbHLH057 enhanced rice disease resistance to fungus Rhizoctonia solani and drought tolerance [138]. In sorghum, a typical bHLH gene, SbbHLH85, plays a key role in the root development, and its overexpression increased Na+ absorption, which indicates that SbbHLH85 might play a negative regulatory role in salt tolerance [87].
The ectopic expression of CabHLH035 in pepper (Capsicum annuum L.) enhanced the salt tolerance in transgenic Arabidopsis [139]. The overexpression of MxbHLH18 in apple increased iron and high-salinity stress tolerances in Arabidopsis [140]. Zuo et al. [34] reported the genome-wide identification of the bHLH family genes in Zoysia japonica. The expressions of ZjbHLH62/ZjICE2, ZjbHLH67, ZjbHLH76/ZjICE1, ZjbHLH88, ZjbHLH97, and ZjbHLH120 in subfamily IIIb were affected by cold, salt, dehydration, and/or ABA [34]. Furthermore, the overexpression of ZjICE1 and ZjICE2 endowed transgenic Arabidopsis and Z. japonica plants with abiotic stress tolerance via the activation of the DREB/CBF regulon, and they also enhanced ROS scavenging [141,142]. The overexpression of MfbHLH38, which is a bHLH gene of Myrothamnus flabellifolia, increased the tolerance to drought and salt stresses in transgenic Arabidopsis [143]. HbICE2, which is a novel ICE-like gene in the rubber tree (Hevea brasiliensis), is involved in JA-mediated cold tolerance and its overexpression enhanced the cold resistance in transgenic Arabidopsis [144]. The ThbHLH1 (subfamily XI) plays an important role in stress signaling pathways and induces the expressions of stress-related genes [145]. The bHLH transcription factors regulate a wide range of plant growth and stress response signaling pathways, and some of them share homeopathic pathways for plant survival under unfavorable or stressful conditions.
Metal deficiency (iron) substantially affects many physiological processes of plants, such as photosynthesis and respiration. Both low and high concentrations of iron greatly affect the growth of plants. Plants have developed regulatory systems to control their iron uptake and maintain their Fe homeostasis, and bHLH transcription factors play important roles in this process [146]. In rice, the Iron-related transcription factor 3 (OsIRO3) in subfamily IVb is upregulated by environmental stress, and OsIRO3 is characterized as a negative regulator. The overexpression of OsIRO3 reduced the gene expression in the process of Fe chelator biosynthesis that included OsIRO2 [147]. Wang et al. [148] demonstrated that OsIRO3 formed both homodimers and heterodimers with the subgroup IVb bHLH transcription factor OsbHLH06 that is involved in the transcriptional repression processes in complex networks. Furthermore, researchers have also identified upstream positive bHLH regulators of OsIRO3 in iron homeostasis, such as Photochemical Reflectance Index 1 (OsPRI1), OsPRI2/OsbHLH58 and OsPRI3/OsbHLH59, which are in subfamily IVc (Figure 2) [149,150]. OsbHLH133, in the subfamily VIIIc(2), plays an important role in the Fe-deficiency signaling network under Fe-deficient conditions in rice [151]. We present the results for other species, such as soybean, and apple, in Table 1. Manganese (Mn) is also an essential micro-nutrient that acts as a cofactor in the redox reactions in photosynthesis. ZmbHLH105 confers improved Mn tolerance on the transgenic tobacco by repressing the expressions of the Mn/Fe-regulated transporter genes to reduce the Mn acclamation [152].
In summary, plant growth is strictly controlled by intricate regulation mechanisms, and the bHLH family genes always function with many other proteins to allow plants to perform specific developmental processes at suitable times, and to increase their chances of survival under unfavorable environments. Various research studies have demonstrated that bHLH transcription factors play important roles in a broad range of plant growth and developmental processes via crosstalk. For example, RERJ1 mediates the defense processes against herbivory and bacterial infection through JA signaling [124], OsPIL11 and OsPIL16 are involved in photomorphogenic developmental processes that are affected by light [116], and OsbHLH148 regulates drought stress in rice, which also responds to JA treatment [134]. The establishment of this mechanism is complicated, and systematic investigations into the bHLH genes in plants will facilitate their use for crop improvement programs.
Table
Table 1. Functional characterization of basic helix-loop-helix (bHLH) proteins.
Table 1. Functional characterization of basic helix-loop-helix (bHLH) proteins.
SubfamilyGene NameGene AccessionContributionReference
II
ClATM1Cla010576Anther development[73]
OsEAT1Os04g0599300Anther development[68]
OsTIP2Os01g0293100Anther development[67]
SlMS10Solyc02g079810Pollen and tapetum development[75]
SlMS32Solyc01g081100Pollen and tapetum development[74]
III(a+c)
CabHLH035LOC107866727Salt[139]
OsRERJOs04t0301500JA signaling[123]
PebHLH35AIG53906Drought[153]
IIIb
BjICE53HQ857208Chilling (4 °C)[154]
HbICE2AOO76749Freezing (−8 °C)[144]
OsICE1Os11g0523700Drought[155]
OsICE2Os01g0928000Freezing (−6 °C)[156]
ZjICE1QBQ01909Freezing (−6 °C), drought, salt[141]
ZjICE2QFQ50795Cold, drought, salt[142]
III(d+e)
FtbHLH2KT737455Chilling (4 °C)[157]
OsMYC2Os10g0575000Insect defense[158]
IIIf
DvIVSBAJ33515Anthocyanin biosynthesis[159]
OsS1Os04t0557500Anthocyanin biosynthesis; JA signaling[98]
PabHLH3KP126521Phenylpropanoid metabolism biosynthesis[103]
PabHLH33KP126523Anthocyanin biosynthesis[103]
PpbHLH3ppa002884mAnthocyanin biosynthesis[102]
StbHLH1JX848660Phenylpropanoid biosynthesis[160]
IVb
OsbHLH062Os07g0628500Iron homeostasis[147]
OsIRO3Os03g0379300Iron homeostasis[147]
IVc
OsPRI1Os08g0138500Iron homeostasis[149]
OsPRI2Os05g0455400Iron homeostasis[150]
OsPRI3Os02g0116600Iron homeostasis[150]
OsbHLH057Os07g0543000Disease resistance, drought[138]
ZmbHLH105AIB05526Mn homeostasis[152]
IVd
OsDPFXM_015775745Diterpenoid phytoalexin biosynthetic[104]
OsbHLH024Os01g0575200Salt[136]
OsbHLH148NM_123731Drought; JA signaling[134]
SlAHKR076778Anthocyanin biosynthesis[100]
Va
MfbHLH38QNN83755Salt[143]
Vb
OsbHLH035Os01g0159800Anther development[71]
VII(a+b)
OsbHLH107Os02g0805250Grain development[79]
OsPIL11Os12g0610200light signaling[116]
OsPIL15Os01g0286100Grain development; light signaling[78]
OsPIL16Os05g0139100Grain development; light signaling[77]
VIIIb
ZmbHLH121GRMZM5G868618Kernel development[80]
VIIIc(1)
BdRSL1XM-003565193Root hair development[86]
BdRSL2KQK00978Root hair development[86]
BdRSL3XP-010229851Root hair development [86]
OsRSL1NP-001047894Root hair development[85]
OsRSL2BAF03719Root hair development[85]
OsRSL3BAD46515Root hair development[85]
VIIIc(2)
OsbHLH133Os12g0508500Iron distribution[151]
SbbHLH85SORBI_3008G147800Root hair development[87]
X
AaMYC2-LikeMH820174JA signaling and Artemisinin biosynthesis[125]
OsbHLH130Os09g0487900Drought[137]
XI
ThbHLH1KM101094Salt, osmotic stress[145]
Orphans
SlARSolyc12g098620Carotenoid biosynthesis[105]
LoUDT1MW357612Anther development[72]
OsUDT1Os07g0549600Anther development[69]
Note: JA indicates Jasmonate. The abbreviations of the gene name from different species are showed as below: Aa refers to Artemisia annua L.; Bd refers to Brachypodium distachyon; Bj refers to Brassica juncea; Ca refers to Capsicum annuum L.; Cl refers to Citrullus lanatus L.; Dv refers to Dahlia variabilis; Ft refers to Fagopyrum tataricum; Hb refers to Hevea brasiliensis; Lo refers to Lilium oriental; Mf refers to Myrothamnus flabellifolia; Os refers to Oryza sativa; Pa refers to Prunus avium L.; Pe refers to Populus euphratica; Pp refers to Prunus persica; Sb refers to Sorghum bicolor; Sl refers to Solanum lycopersicum L.; St refers to Solanum tuberosum; Th refers to Tamarix hispida; Zm refers to Zea mays; Zj refers to Zoysia japonica.

3. Conclusions and Perspectives

Genetically modified organisms (GMO) have been widely developed using genetic engineering techniques to alter their original characteristics, such as flower color and shape, or tolerance for biotic and abiotic stresses. Transcription factors regulate different routes by modulating the respective downstream target genes, which can involve multiple plant physiological processes. Therefore, transcription factors are likely better targets for genetic engineering due to their broader regulatory capacities compared with other proteins. The identification of the bHLH transcription factors in different pathways contributes to our comprehensive understanding of the various aspects of plant morphogenesis and adaptation to extreme environments. In Arabidopsis, excellent reviews have covered the roles of bHLH transcription factors from different aspects, which include how bHLH transcription factors mediate Arabidopsis growth and development, such as flowering time control, seed dormancy and germination, and cell fate determination, how they function in environmental responses, such as iron homeostasis regulation, and abiotic stress responses, and how they respond to light and phytohormones [65]. Some bHLH transcription factors play crucial roles in many aspects in the crosstalk pathway, such as BEEs responding to brassinosteroids to regulate normal gynoecium development [17]. In this review, based on the functions of bHLH transcription factors, we classify the bHLH family that from important economic crops into four major categories (plant growth and development; metabolism biosynthesis; plant signaling, and plant abiotic stress), and we demonstrate that the bHLH family transcription factors play vital roles in plant growth, development, and adaptation to environmental stresses.
bHLH transcription factors regulate several pathways, and bHLH transcription factors in the same subfamily can make different contributions within plants. For example, subfamily VIIIc is mainly involved in root hair development, and OsbHLH133 in subfamily VIIIc(2) plays an important role in the Fe-deficiency signaling network, which raises the question as to whether there is a relationship between root hair development and the Fe-deficiency signaling pathways. Whether OsbHLH133 has any potential functions in root hair development is still unknown and poorly understood. Thus, bHLH members in the same subfamily may perform similar functions, but not necessarily. Our current knowledge of the bHLH transcription factors from different species mainly includes gene identification, and researchers have performed most of the functional characterizations in model plants (Arabidopsis or rice). Thus, the knowledge of the mechanisms that underlies these differences is still limited. The bHLH transcription factors from many economically important crops are not well characterized. In this review, we summarize the current research on the bHLH function in rice and other economical plants through an evolutionary classification, not only providing a relatively complete overview of the bHLH transcription factor family, but also indicating the potential functions of the bHLH transcription factors in different subfamilies. This review enriches our understanding of the bHLH family in rice, and it provides new insights into the bHLH transcription factor regulation in various biological processes.
Using genetic engineering tools to improve agronomic traits of crops is an efficient and rapid way for plant molecular breeding. Some bHLH transcription factors have been engineered in transgenic plants to increase plant tolerance, such as drought [134]. In addition, the regulatory capacity of transcription factor genes makes them better targets for genetic engineering, and they have high potential to produce broader responses compared with other proteins. In future studies, researchers should elucidate the mechanism of bHLH protein-regulated plant growth and development via the coordination of multiple pathways, such as phytohormones and environmental factors. In addition, the creation of genetically modified mutants and genetic manipulations of bHLH genes to identify additional regulation pathways in this complex process are also needed. Notably, most bHLH transcription factors that have been functionally investigated so far are evolutionary conserved, whereas the species-specific or tissue-specific bHLH transcription factors have been studied rarely. Thus, much more work is required to decipher the regulatory mechanisms of non-conserved bHLH transcription factors in plant growth, development, and response to biotic or abiotic stresses stimuli. Furthermore, new biotechnological tools will accelerate these complex processes, such as RNAi, virus-induced gene silencing (VIGS), the CRISPR/Cas9 gene editing system, single cell RNA sequencing, and omics analysis. Thus, the future seems bright with respect to the development of crops with improved agronomic traits that use bHLH transcription factors with a greater efficiency than ever before. Therefore, characterization of the bHLH transcription factors in various crops will enrich our understanding of their roles and evolution in plants, and provide new strategies for their genetic applications for plant engineering.

Author Contributions

Z.-F.Z. and H.-G.K. wrote the manuscript. H.-Y.L. provided the critical comments and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) of the Ministry of Education (2019R1A6A1A11052070), Republic of Korea.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available from the authors on request.

Acknowledgments

We thank Adhimoolam Karthikeyan for critical proofreading and reviewers’ valuable suggestions to improve the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Riechmann, J.L.; Ratcliffe, O.J. A genomic perspective on plant transcription factors. Curr. Opin. Plant Biol. 2000, 3, 423–434. [Google Scholar] [CrossRef] [PubMed]
  2. Heim, M.A.; Jakoby, M.; Werber, M.; Martin, C.; Weisshaar, B.; Bailey, P.C. The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 2003, 20, 735–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Ledent, V.; Vervoort, M. The basic helix-loop-helix protein family: Comparative genomics and phylogenetic analysis. Genome Res. 2001, 11, 754–770. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Ferré-D’Amaré, A.R.; Prendergast, G.C.; Ziff, E.B.; Burley, S.K. Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 1993, 363, 38–45. [Google Scholar] [CrossRef]
  5. Pires, N.; Dolan, L. Origin and diversification of basic-helix-loop-helix proteins in plants. Mol. Biol. Evol. 2010, 27, 862–874. [Google Scholar] [CrossRef] [Green Version]
  6. Atchley, W.R.; Terhalle, W.; Dress, A. Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J. Mol. Evol. 1999, 48, 501–516. [Google Scholar] [CrossRef]
  7. Atchley, W.R.; Fitch, W.M. A natural classification of the basic helix–loop–helix class of transcription factors. Proc. Natl. Acad. Sci. USA 1997, 94, 5172–5176. [Google Scholar] [CrossRef] [Green Version]
  8. Ledent, V.; Paquet, O.; Vervoort, M. Phylogenetic analysis of the human basic helix-loop-helix proteins. Genome Biol. 2002, 3, research0030.1. [Google Scholar] [CrossRef] [Green Version]
  9. Carretero-Paulet, L.; Galstyan, A.; Roig-Villanova, I.; Martínez-García, J.F.; Bilbao-Castro, J.R.; Robertson, D.L. Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol. 2010, 153, 1398–1412. [Google Scholar] [CrossRef] [Green Version]
  10. Kondou, Y.; Nakazawa, M.; Kawashima, M.; Ichikawa, T.; Yoshizumi, T.; Suzuki, K.; Ishikawa, A.; Koshi, T.; Matsui, R.; Muto, S. RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol. 2008, 147, 1924–1935. [Google Scholar] [CrossRef]
  11. Gremski, K.; Ditta, G.; Yanofsky, M.F. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 2007, 134, 3593–3601. [Google Scholar] [CrossRef] [Green Version]
  12. Zhang, W.; Sun, Y.; Timofejeva, L.; Chen, C.; Grossniklaus, U.; Ma, H. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 2006, 133, 3085–3095. [Google Scholar] [CrossRef] [Green Version]
  13. Liljegren, S.J.; Roeder, A.H.; Kempin, S.A.; Gremski, K.; Østergaard, L.; Guimil, S.; Reyes, D.K.; Yanofsky, M.F. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 2004, 116, 843–853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Rajani, S.; Sundaresan, V. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 2001, 11, 1914–1922. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Nesi, N.; Debeaujon, I.; Jond, C.; Pelletier, G.; Caboche, M.; Lepiniec, L. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 2000, 12, 1863–1878. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Castillon, A.; Shen, H.; Huq, E. Phytochrome interacting factors: Central players in phytochrome-mediated light signaling networks. Trends Plant Sci. 2007, 12, 514–521. [Google Scholar] [CrossRef]
  17. Friedrichsen, D.M.; Nemhauser, J.; Muramitsu, T.; Maloof, J.N.; Alonso, J.; Ecker, J.R.; Furuya, M.; Chory, J. Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 2002, 162, 1445–1456. [Google Scholar] [CrossRef]
  18. Ali, A.; Javed, T.; Zaheer, U.; Zhou, J.R.; Huang, M.T.; Fu, H.Y.; Gao, S.J. Genome-wide identification and expression profiling of the bHLH transcription factor gene family in Saccharum spontaneum under bacterial pathogen stimuli. Trop. Plant Biol. 2021, 14, 283–294. [Google Scholar] [CrossRef]
  19. Chinnusamy, V.; Ohta, M.; Kanrar, S.; Lee, B.-H.; Hong, X.; Agarwal, M.; Zhu, J.-K. ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003, 17, 1043–1054. [Google Scholar] [CrossRef] [Green Version]
  20. Fursova, O.V.; Pogorelko, G.V.; Tarasov, V.A. Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 2009, 429, 98–103. [Google Scholar] [CrossRef]
  21. Ariyarathne, M.A.; Wone, B.W. Overexpression of the Selaginella lepidophylla bHLH transcription factor enhances water-use efficiency, growth, and development in Arabidopsis. Plant Sci. 2022, 315, 111129. [Google Scholar] [CrossRef] [PubMed]
  22. Toledo-Ortiz, G.; Huq, E.; Quail, P.H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 2003, 15, 1749–1770. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Li, X.; Duan, X.; Jiang, H.; Sun, Y.; Tang, Y.; Yuan, Z.; Guo, J.; Liang, W.; Chen, L.; Yin, J. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol. 2006, 141, 1167–1184. [Google Scholar] [CrossRef] [Green Version]
  24. Simionato, E.; Ledent, V.; Richards, G.; Thomas-Chollier, M.; Kerner, P.; Coornaert, D.; Degnan, B.M.; Vervoort, M. Origin and diversification of the basic helix-loop-helix gene family in metazoans: Insights from comparative genomics. BMC Evol. Biol. 2007, 7, 33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Robinson, K.A.; Lopes, J.M. SURVEY AND SUMMARY: Saccharomyces cerevisiae basic helix-loop-helix proteins regulate diverse biological processes. Nucleic Acids Res. 2000, 28, 1499–1505. [Google Scholar] [CrossRef] [PubMed]
  26. Zhou, X.; Liao, Y.; Kim, S.-U.; Chen, Z.; Nie, G.; Cheng, S.; Ye, J.; Xu, F. Genome-wide identification and characterization of bHLH family genes from Ginkgo biloba. Sci. Rep. 2020, 10, 1–15. [Google Scholar]
  27. Aslam, M.; Jakada, B.H.; Fakher, B.; Greaves, J.G.; Niu, X.; Su, Z.; Cheng, Y.; Cao, S.; Wang, X.; Qin, Y. Genome-wide study of pineapple (Ananas comosus L.) bHLH transcription factors indicates that cryptochrome-interacting bHLH2 (AcCIB2) participates in flowering time regulation and abiotic stress response. BMC Genom. 2020, 21, 735. [Google Scholar]
  28. Lu, X.; Zhang, H.; Hu, J.; Nie, G.; Khan, I.; Feng, G.; Zhang, X.; Wang, X.; Huang, L. Genome-wide identification and characterization of bHLH family genes from orchardgrass and the functional characterization of DgbHLH46 and DgbHLH128 in drought and salt tolerance. Funct. Integr. Genomics 2022, 22, 1331–1344. [Google Scholar]
  29. Li, C.; Cai, X.; Shen, Q.; Chen, X.; Xu, M.; Ye, T.; Si, D.; Wu, L.; Chen, D.; Han, Z. Genome-wide analysis of basic helix-loop-helix genes in Dendrobium catenatum and functional characterization of DcMYC2 in jasmonate-mediated immunity to Sclerotium delphinii. Front. Plant Sci. 2022, 13, 956210. [Google Scholar] [CrossRef]
  30. Ke, Q.; Tao, W.; Li, T.; Pan, W.; Chen, X.; Wu, X.; Nie, X.; Cui, L. Genome-wide identification, evolution and expression analysis of basic helix-loop-helix (bHLH) gene family in barley (Hordeum vulgare L.). Curr. Genomics 2020, 21, 624–644. [Google Scholar] [CrossRef]
  31. Cheng, X.; Xiong, R.; Liu, H.; Wu, M.; Chen, F.; Yan, H.; Xiang, Y. Basic helix-loop-helix gene family: Genome wide identification, phylogeny, and expression in Moso bamboo. Plant Physiol. Biochem. 2018, 132, 104–119. [Google Scholar] [CrossRef] [PubMed]
  32. Wang, Z.; Jia, C.; Wang, J.-Y.; Miao, H.-X.; Liu, J.-H.; Chen, C.; Yang, H.-X.; Xu, B.; Jin, Z. Genome-wide analysis of basic helix-loop-helix transcription factors to elucidate candidate genes related to fruit ripening and stress in Banana (Musa acuminata L. AAA Group, cv. Cavendish). Front. Plant Sci. 2020, 11, 650. [Google Scholar] [CrossRef]
  33. Wang, L.; Xiang, L.; Hong, J.; Xie, Z.; Li, B. Genome-wide analysis of bHLH transcription factor family reveals their involvement in biotic and abiotic stress responses in wheat (Triticum aestivum L.). 3 Biotech 2019, 9, 1–12. [Google Scholar] [CrossRef]
  34. Zuo, Z.-F.; Sun, H.-J.; Lee, H.-Y.; Kang, H.-G. Identification of bHLH genes through genome-wide association study and antisense expression of ZjbHLH076/ZjICE1 influence tolerance to low temperature and salinity in Zoysia japonica. Plant Sci. 2021, 313, 111088. [Google Scholar] [CrossRef]
  35. Xu, J.; Xu, H.; Zhao, H.; Liu, H.; Xu, L.; Liang, Z. Genome-wide investigation of bHLH genes and expression analysis under salt and hormonal treatments in Andrographis paniculata. Ind. Crops Prod. 2022, 183, 114928. [Google Scholar] [CrossRef]
  36. Li, X.; Huang, H.; Zhang, Z.-Q. Genome-wide identification and expression analysis of bHLH transcription factors reveal their putative regulatory effects on petal nectar spur development in Aquilegia. bioRxiv 2022. [Google Scholar] [CrossRef]
  37. Sun, P.-W.; Gao, Z.-H.; Lv, F.-F.; Yu, C.-C.; Jin, Y.; Xu, Y.-H.; Wei, J.-H. Genome-wide analysis of basic helix-loop-helix (bHLH) transcription factors in Aquilaria sinensis. Sci. Rep. 2022, 12, 1–11. [Google Scholar]
  38. Gao, C.; Sun, J.; Wang, C.; Dong, Y.; Xiao, S.; Wang, X.; Jiao, Z. Genome-wide analysis of basic/helix-loop-helix gene family in peanut and assessment of its roles in pod development. PLoS One 2017, 12, e0181843. [Google Scholar] [CrossRef] [Green Version]
  39. Suchithra, B. Genome-wide analysis of bHLH and bZIP Transcription factors and their temporal expression under abiotic stress conditions in Groundnut (Arachis hypogaea L.). J. Stress Physiol. Biochem. 2022, 18, 47–75. [Google Scholar]
  40. Song, X.-M.; Huang, Z.-N.; Duan, W.-K.; Ren, J.; Liu, T.-K.; Li, Y.; Hou, X.-L. Genome-wide analysis of the bHLH transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol. Genet. Genom. 2014, 289, 77–91. [Google Scholar]
  41. Hong, Y.; Ahmad, N.; Tian, Y.; Liu, J.; Wang, L.; Wang, G.; Liu, X.; Dong, Y.; Wang, F.; Liu, W. Genome-wide identification, expression analysis, and subcellular localization of Carthamus tinctorius bHLH transcription factors. Int. J. Mol. Sci. 2019, 20, 3044. [Google Scholar] [CrossRef] [Green Version]
  42. Chen, Y.-Y.; Li, M.-Y.; Wu, X.-J.; Huang, Y.; Ma, J.; Xiong, A.-S. Genome-wide analysis of basic helix-loop-helix family transcription factors and their role in responses to abiotic stress in carrot. Mol. Breed. 2015, 35, 1–12. [Google Scholar] [CrossRef]
  43. Zhang, S.-X.; Wu, S.-H.; Chao, J.-Q.; Yang, S.-G.; Bao, J.; Tian, W.-M. Genome-wide identification and expression analysis of MYC transcription factor family genes in rubber tree (Hevea brasiliensis Muell. Arg.). Forests 2022, 13, 531. [Google Scholar] [CrossRef]
  44. Ni, L.; Wang, Z.; Fu, Z.; Liu, D.; Yin, Y.; Li, H.; Gu, C. Genome-wide analysis of basic helix-loop-helix family genes and expression analysis in response to drought and salt stresses in Hibiscus hamabo Sieb. et Zucc. Int. J. Mol. Sci. 2021, 22, 8748. [Google Scholar] [CrossRef]
  45. Zhang, L.; Chen, W.; Liu, R.; Shi, B.; Shu, Y.; Zhang, H. Genome-wide characterization and expression analysis of bHLH gene family in physic nut (Jatropha curcas L.). PeerJ 2022, 10, e13786. [Google Scholar] [CrossRef]
  46. Li, R.; Ahmad, B.; Hwarari, D.; Li, D.a.; Lu, Y.; Gao, M.; Chen, J.; Yang, L. Genomic survey and cold-induced expression patterns of bHLH transcription factors in Liriodendron chinense (Hemsl) Sarg. Forests 2022, 13, 518. [Google Scholar] [CrossRef]
  47. An, F.; Xiao, X.; Chen, T.; Xue, J.; Luo, X.; Ou, W.; Li, K.; Cai, J.; Chen, S. Systematic analysis of bHLH transcription factors in cassava uncovers their roles in postharvest physiological deterioration and cyanogenic glycosides biosynthesis. Front. Plant Sci. 2022, 13, 901128. [Google Scholar]
  48. Salih, H.; Tan, L.; Htet, N.N.W. Genome-Wide identification, characterization of bHLH transcription factors in mango. Trop. Plant Res. 2021, 14, 72–81. [Google Scholar]
  49. Ndayambaza, B.; Jin, X.; Min, X.; Lin, X.; Yin, X.; Liu, W. Genome-wide identification and expression analysis of the barrel medic (Medicago truncatula) and alfalfa (Medicago sativa L.) basic helix-loop-helix transcription factor family under salt and drought stresses. J. Plant Growth Regul. 2021, 40, 2058–2078. [Google Scholar] [CrossRef]
  50. Mao, T.-Y.; Liu, Y.-Y.; Zhu, H.-H.; Zhang, J.; Yang, J.-X.; Fu, Q.; Wang, N.; Wang, Z. Genome-wide analyses of the bHLH gene family reveals structural and functional characteristics in the aquatic plant Nelumbo nucifera. PeerJ 2019, 7, e7153. [Google Scholar] [CrossRef] [Green Version]
  51. Li, Y.; Li, L.; Ding, W.; Li, H.; Shi, T.; Yang, X.; Wang, L.; Yue, Y. Genome-wide identification of Osmanthus fragrans bHLH transcription factors and their expression analysis in response to abiotic stress. Environ. Exp. Bot. 2020, 172, 103990. [Google Scholar]
  52. Chu, Y.; Xiao, S.; Su, H.; Liao, B.; Zhang, J.; Xu, J.; Chen, S. Genome-wide characterization and analysis of bHLH transcription factors in Panax ginseng. Acta Pharm. Sin. B 2018, 8, 666–677. [Google Scholar] [CrossRef] [PubMed]
  53. Wang, X.-J.; Peng, X.-Q.; Shu, X.-C.; Li, Y.-H.; Wang, Z.; Zhuang, W.-B. Genome-wide identification and characterization of PdbHLH transcription factors related to anthocyanin biosynthesis in colored-leaf poplar (Populus deltoids). BMC Genom. 2022, 23, 244. [Google Scholar] [CrossRef] [PubMed]
  54. Ye, Y.; Xin, H.; Gu, X.; Ma, J.; Li, L. Genome-wide identification and functional analysis of the Basic Helix-Loop-Helix (bHLH) transcription family reveals candidate PtFBH genes involved in the flowering process of Populus trichocarpa. Forests 2021, 12, 1439. [Google Scholar] [CrossRef]
  55. Shen, T.; Wen, X.; Wen, Z.; Qiu, Z.; Hou, Q.; Li, Z.; Mei, L.; Yu, H.; Qiao, G. Genome-wide identification and expression analysis of bHLH transcription factor family in response to cold stress in sweet cherry (Prunus avium L.). Sci. Hortic. 2021, 279, 109905. [Google Scholar] [CrossRef]
  56. Wu, Y.; Wu, S.; Wang, X.; Mao, T.; Bao, M.; Zhang, J.; Zhang, J. Genome-wide identification and characterization of the bHLH gene family in an ornamental woody plant Prunus mume. Hortic. Plant J. 2022, 8, 531–544. [Google Scholar] [CrossRef]
  57. Zhang, C.; Feng, R.; Ma, R.; Shen, Z.; Cai, Z.; Song, Z.; Peng, B.; Yu, M. Genome-wide analysis of basic helix-loop-helix superfamily members in peach. PloS One 2018, 13, e0195974. [Google Scholar] [CrossRef]
  58. Xiao, L.; Huang, D.; Wu, Z.; Shang, X.; Cao, S.; Zeng, W.; Lu, L.; Shi, P.; Yan, H. Genome-Wide Snalysis of the bHLH Transcription Factor Family and Functional Identification of bHLH Genes Related to Puerarin Biosynthesis in Pueraria lobata var. thomsonii (Benth.). 2022. Available online: https://www.researchsquare.com/article/rs-1703982/v1 (accessed on 10 August 2022).
  59. Wang, R.; Li, Y.; Gao, M.; Han, M.; Liu, H. Genome-wide identification and characterization of the bHLH gene family and analysis of their potential relevance to chlorophyll metabolism in Raphanus sativus L. BMC Genom. 2022, 23, 548. [Google Scholar]
  60. Zhang, X.; Luo, H.; Xu, Z.; Zhu, Y.; Ji, A.; Song, J.; Chen, S. Genome-wide characterisation and analysis of bHLH transcription factors related to tanshinone biosynthesis in Salvia miltiorrhiza. Sci. Rep. 2015, 5, 11244. [Google Scholar]
  61. Sun, H.; Fan, H.-J.; Ling, H.-Q. Genome-wide identification and characterization of the bHLH gene family in tomato. BMC Genom. 2015, 16, 1–12. [Google Scholar] [CrossRef] [Green Version]
  62. Wang, R.; Zhao, P.; Kong, N.; Lu, R.; Pei, Y.; Huang, C.; Ma, H.; Chen, Q. Genome-wide identification and characterization of the potato bHLH transcription factor family. Genes 2018, 9, 54. [Google Scholar] [CrossRef] [PubMed]
  63. Wei, X.; Cao, J.; Lan, H. Genome-wide characterization and analysis of the bHLH transcription factor family in Suaeda aralocaspica, an annual halophyte with single-cell C4 anatomy. Front. Plant Sci. 2022, 13, 927830. [Google Scholar] [CrossRef]
  64. Lang, Y.; Liu, Z. Basic Helix-Loop-Helix (bHLH) transcription factor family in Yellow horn (Xanthoceras sorbifolia Bunge): Genome-wide characterization, chromosome location, phylogeny, structures and expression patterns. Int. J. Biol. Macromol. 2020, 160, 711–723. [Google Scholar] [CrossRef] [PubMed]
  65. Hao, Y.; Zong, X.; Ren, P.; Qian, Y.; Fu, A. Basic Helix-Loop-Helix (bHLH) transcription factors regulate a wide range of functions in Arabidopsis. Int. J. Mol. Sci. 2021, 22, 7152. [Google Scholar] [CrossRef] [PubMed]
  66. Laza, H.E.; Kaur-Kapoor, H.; Xin, Z.; Payton, P.R.; Chen, J. Morphological analysis and stage determination of anther development in Sorghum [Sorghum bicolor (L.) Moench]. Planta 2022, 255, 86. [Google Scholar] [CrossRef] [PubMed]
  67. Fu, Z.; Yu, J.; Cheng, X.; Zong, X.; Xu, J.; Chen, M.; Li, Z.; Zhang, D.; Liang, W. The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 2014, 26, 1512–1524. [Google Scholar] [CrossRef] [Green Version]
  68. Niu, N.; Liang, W.; Yang, X.; Jin, W.; Wilson, Z.A.; Hu, J.; Zhang, D. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 2013, 4, 1455. [Google Scholar] [CrossRef] [Green Version]
  69. Jung, K.-H.; Han, M.-J.; Lee, Y.-S.; Kim, Y.-W.; Hwang, I.; Kim, M.-J.; Kim, Y.-K.; Nahm, B.H.; An, G. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 2005, 17, 2705–2722. [Google Scholar] [CrossRef] [Green Version]
  70. Ono, S.; Liu, H.; Tsuda, K.; Fukai, E.; Tanaka, K.; Sasaki, T.; Nonomura, K.-I. EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogenesis in rice anther tapetum. PLoS Genet. 2018, 14, e1007238. [Google Scholar] [CrossRef]
  71. Ortolan, F.; Fonini, L.S.; Pastori, T.; Mariath, J.E.; Saibo, N.J.; Margis-Pinheiro, M.; Lazzarotto, F. Tightly controlled expression of OsbHLH35 is critical for anther development in rice. Plant Sci. 2021, 302, 110716. [Google Scholar] [CrossRef]
  72. Yuan, G.; Wu, Z.; Liu, X.; Li, T.; Teng, N. Characterization and functional analysis of LoUDT1, a bHLH transcription factor related to anther development in the lily oriental hybrid Siberia (Lilium spp.). Plant Physiol. Biochem. 2021, 166, 1087–1095. [Google Scholar] [CrossRef] [PubMed]
  73. Zhang, R.; Chang, J.; Li, J.; Lan, G.; Xuan, C.; Li, H.; Ma, J.; Zhang, Y.; Yang, J.; Tian, S. Disruption of the bHLH transcription factor Abnormal Tapetum 1 causes male sterility in watermelon. Hortic. Res. 2021, 8, 258. [Google Scholar] [CrossRef]
  74. Liu, X.; Yang, M.; Liu, X.; Wei, K.; Cao, X.; Wang, X.; Wang, X.; Guo, Y.; Du, Y.; Li, J. A putative bHLH transcription factor is a candidate gene for male sterile 32, a locus affecting pollen and tapetum development in tomato. Hortic. Res. 2019, 6, 88. [Google Scholar] [CrossRef] [Green Version]
  75. Jung, Y.J.; Kim, D.H.; Lee, H.J.; Nam, K.H.; Bae, S.; Nou, I.S.; Cho, Y.-G.; Kim, M.K.; Kang, K.K. Knockout of SlMS10 gene (Solyc02g079810) encoding bHLH transcription factor using CRISPR/Cas9 System confers male sterility phenotype in tomato. Plants 2020, 9, 1189. [Google Scholar] [CrossRef]
  76. Heang, D.; Sassa, H. An atypical bHLH protein encoded by POSITIVE REGULATOR OF GRAIN LENGTH 2 is involved in controlling grain length and weight of rice through interaction with a typical bHLH protein APG. Breed. Sci. 2012, 62, 133–141. [Google Scholar] [CrossRef] [Green Version]
  77. Heang, D.; Sassa, H. Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS ONE 2012, 7, e31325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Ji, X.; Du, Y.; Li, F.; Sun, H.; Zhang, J.; Li, J.; Peng, T.; Xin, Z.; Zhao, Q. The basic helix-loop-helix transcription factor, OsPIL15, regulates grain size via directly targeting a purine permease gene OsPUP7 in rice. Plant Biotechnol. J. 2019, 17, 1527–1537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Yang, X.; Ren, Y.; Cai, Y.; Niu, M.; Feng, Z.; Jing, R.; Mou, C.; Liu, X.; Xiao, L.; Zhang, X. Overexpression of OsbHLH107, a member of the basic helix-loop-helix transcription factor family, enhances grain size in rice (Oryza sativa L.). Rice 2018, 11, 41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Das, A.K.; Hao, L. Functional characterization of ZmbHLH121, a bHLH transcription factor, focusing on Zea mays kernel development. Gene Rep. 2022, 28, 101645. [Google Scholar] [CrossRef]
  81. Bibikova, T.; Gilroy, S. Root hair development. J. Plant Growth Regul. 2002, 21, 383–415. [Google Scholar]
  82. Schiefelbein, J.W. Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 2000, 124, 1525–1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Datta, S.; Kim, C.M.; Pernas, M.; Pires, N.D.; Proust, H.; Tam, T.; Vijayakumar, P.; Dolan, L. Root hairs: Development, growth and evolution at the plant-soil interface. Plant Soil 2011, 346, 205–212. [Google Scholar] [CrossRef]
  84. Gilroy, S.; Jones, D.L. Through form to function: Root hair development and nutrient uptake. Trends Plant Sci. 2000, 5, 56–60. [Google Scholar] [CrossRef]
  85. Kim, C.M.; Han, C.d.; Dolan, L. RSL class I genes positively regulate root hair development in Oryza sativa. New Phytol. 2017, 213, 314–323. [Google Scholar] [CrossRef]
  86. Kim, C.M.; Dolan, L. ROOT HAIR DEFECTIVE SIX-LIKE class I genes promote root hair development in the grass Brachypodium distachyon. PLoS Genet. 2016, 12, e1006211. [Google Scholar]
  87. Song, Y.; Li, S.; Sui, Y.; Zheng, H.; Han, G.; Sun, X.; Yang, W.; Wang, H.; Zhuang, K.; Kong, F. SbbHLH85, a bHLH member, modulates resilience to salt stress by regulating root hair growth in sorghum. Theor. Appl. Genet. 2022, 135, 201–216. [Google Scholar] [CrossRef]
  88. Dixon, R.A.; Xie, D.Y.; Sharma, S.B. Proanthocyanidins—A final frontier in flavonoid research? New Phytol. 2005, 165, 9–28. [Google Scholar] [CrossRef] [Green Version]
  89. Saltveit, M.E. Synthesis and metabolism of phenolic compounds. Fruit Veget. Phytochem. Chem. 2017, 2, 115. [Google Scholar]
  90. Petroni, K.; Tonelli, C. Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci. 2011, 181, 219–229. [Google Scholar] [CrossRef]
  91. Samanta, A.; Das, G.; Das, S.K. Roles of flavonoids in plants. Carbon 2011, 100, 12–35. [Google Scholar]
  92. Miguel, M.G. Anthocyanins: Antioxidant and/or anti-inflammatory activities. J. Appl. Pharm. Sci. 2011, 1, 7–15. [Google Scholar]
  93. Khoo, H.E.; Azlan, A.; Tang, S.T.; Lim, S.M. Anthocyanidins and anthocyanins: Colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food Nutr. Res. 2017, 61, 1361779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Gündeşli, M.A.; Korkmaz, N.; Okatan, V. Polyphenol content and antioxidant capacity of berries: A review. Int. J. Agric. For. Life Sci. 2019, 3, 350–361. [Google Scholar]
  95. Hichri, I.; Barrieu, F.; Bogs, J.; Kappel, C.; Delrot, S.; Lauvergeat, V. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 2011, 62, 2465–2483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Patra, B.; Schluttenhofer, C.; Wu, Y.; Pattanaik, S.; Yuan, L. Transcriptional regulation of secondary metabolite biosynthesis in plants. Biochim. Biophys. Acta Gene Regul. Mech. 2013, 1829, 1236–1247. [Google Scholar] [CrossRef] [PubMed]
  97. Jaakola, L. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci. 2013, 18, 477–483. [Google Scholar] [CrossRef] [Green Version]
  98. Sun, X.; Zhang, Z.; Li, J.; Zhang, H.; Peng, Y.; Li, Z. Uncovering hierarchical regulation among MYB-bHLH-WD40 proteins and manipulating anthocyanin pigmentation in Rice. Int. J. Mol. Sci. 2022, 23, 8203. [Google Scholar] [CrossRef]
  99. Zhang, Q.; Feng, Y.-X.; Tian, P.; Lin, Y.-J.; Yu, X.-Z. Proline-mediated regulation on jasmonate signals repressed anthocyanin accumulation through the MYB-bHLH-WDR complex in rice under chromium exposure. Front. Plant Sci. 2022, 13, 953398. [Google Scholar] [CrossRef]
  100. Qiu, Z.; Wang, X.; Gao, J.; Guo, Y.; Huang, Z.; Du, Y. The tomato Hoffman’s Anthocyaninless gene encodes a bHLH transcription factor involved in anthocyanin biosynthesis that is developmentally regulated and induced by low temperatures. PLoS ONE 2016, 11, e0151067. [Google Scholar] [CrossRef] [Green Version]
  101. Li, Y.; Shan, X.; Gao, R.; Yang, S.; Wang, S.; Gao, X.; Wang, L. Two IIIf clade-bHLHs from Freesia hybrida play divergent roles in flavonoid biosynthesis and trichome formation when ectopically expressed in Arabidopsis. Sci. Rep. 2016, 6, 30514. [Google Scholar] [CrossRef]
  102. Rahim, M.A.; Busatto, N.; Trainotti, L. Regulation of anthocyanin biosynthesis in peach fruits. Planta 2014, 240, 913–929. [Google Scholar] [CrossRef]
  103. Starkevič, P.; Paukštytė, J.; Kazanavičiūtė, V.; Denkovskienė, E.; Stanys, V.; Bendokas, V.; Šikšnianas, T.; Ražanskienė, A.; Ražanskas, R. Expression and anthocyanin biosynthesis-modulating potential of sweet cherry (Prunus avium L.) MYB10 and bHLH Genes. PLoS ONE 2015, 10, e0126991. [Google Scholar] [CrossRef] [PubMed]
  104. Yamamura, C.; Mizutani, E.; Okada, K.; Nakagawa, H.; Fukushima, S.; Tanaka, A.; Maeda, S.; Kamakura, T.; Yamane, H.; Takatsuji, H. Diterpenoid phytoalexin factor, a bHLH transcription factor, plays a central role in the biosynthesis of diterpenoid phytoalexins in rice. Plant J. 2015, 84, 1100–1113. [Google Scholar] [CrossRef] [PubMed]
  105. D’Amelia, V.; Raiola, A.; Carputo, D.; Filippone, E.; Barone, A.; Rigano, M.M. A basic Helix-Loop-Helix (SlARANCIO), identified from a Solanum pennellii introgression line, affects carotenoid accumulation in tomato fruits. Sci. Rep. 2019, 9, 3699. [Google Scholar] [CrossRef] [Green Version]
  106. Gyula, P.; Schäfer, E.; Nagy, F. Light perception and signalling in higher plants. Curr. Opin. Plant Biol. 2003, 6, 446–452. [Google Scholar] [CrossRef]
  107. Burgie, E.S.; Vierstra, R.D. Phytochromes: An atomic perspective on photoactivation and signaling. Plant Cell 2014, 26, 4568–4583. [Google Scholar] [CrossRef] [Green Version]
  108. Palayam, M.; Ganapathy, J.; Guercio, A.M.; Tal, L.; Deck, S.L.; Shabek, N. Structural insights into photoactivation of plant Cryptochrome-2. Commun. Biol. 2021, 4, 28. [Google Scholar] [CrossRef] [PubMed]
  109. Goh, C.-H. Phototropins and chloroplast activity in plant blue light signaling. Plant Signal. Behav. 2009, 4, 693–695. [Google Scholar] [CrossRef] [Green Version]
  110. Jeong, J.; Choi, G. Phytochrome-interacting factors have both shared and distinct biological roles. Mol. Cells. 2013, 35, 371–380. [Google Scholar] [CrossRef] [Green Version]
  111. Ordeiro, A.M.; Andrade, L.; Monteiro, C.C.; Leitão, G.; Wigge, P.A.; Saibo, N.J. Phytochrome-Interacting Factors: A promising tool to improve crop productivity. J. Exp. Bot. 2022, 73, 3881–3897. [Google Scholar] [CrossRef]
  112. Cordeiro, A.M.; Figueiredo, D.D.; Tepperman, J.; Borba, A.R.; Lourenço, T.; Abreu, I.A.; Ouwerkerk, P.B.; Quail, P.H.; Oliveira, M.M.; Saibo, N.J. Rice phytochrome-interacting factor protein OsPIF14 represses OsDREB1B gene expression through an extended N-box and interacts preferentially with the active form of phytochrome B. Biochim. Biophy. Acta Gene Regul. Mech. 2016, 1859, 393–404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Nakamura, Y.; Kato, T.; Yamashino, T.; Murakami, M.; Mizuno, T. Characterization of a set of phytochrome-interacting factor-like bHLH proteins in Oryza sativa. Biosci. Biotechnol. Biochem. 2007, 71, 1183–1191. [Google Scholar] [CrossRef] [Green Version]
  114. Zhou, J.; Liu, Q.; Zhang, F.; Wang, Y.; Zhang, S.; Cheng, H.; Yan, L.; Li, L.; Chen, F.; Xie, X. Overexpression of OsPIL15, a phytochrome-interacting factor-like protein gene, represses etiolated seedling growth in rice. J. Integr. Plant Biol. 2014, 56, 373–387. [Google Scholar] [CrossRef]
  115. Xie, C.; Zhang, G.; An, L.; Chen, X.; Fang, R. Phytochrome-interacting factor-like protein OsPIL15 integrates light and gravitropism to regulate tiller angle in rice. Planta 2019, 250, 105–114. [Google Scholar] [CrossRef]
  116. Li, Y.; Zhang, F.; Zheng, C.; Zhou, J.; Meng, X.; Niu, S.; Chen, F.; Zhang, H.; Xie, X. Fusion of the SRDX motif to OsPIL11 or OsPIL16 causes rice constitutively photomorphogenic phenotypes in darkness. Plant Growth Regul. 2022, 96, 157–175. [Google Scholar] [CrossRef]
  117. He, Y.; Li, Y.; Cui, L.; Xie, L.; Zheng, C.; Zhou, G.; Zhou, J.; Xie, X. Phytochrome B negatively affects cold tolerance by regulating OsDREB1 gene expression through phytochrome interacting factor-like protein OsPIL16 in rice. Front. Plant Sci. 2016, 7, 1963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  118. Chen, Y.; Zhang, M.; Wang, Y.; Zheng, X.; Zhang, H.; Zhang, L.; Tan, B.; Ye, X.; Wang, W.; Li, M. PpPIF8, a DELLA2-interacting protein, regulates peach shoot elongation possibly through auxin signaling. Plant Sci. 2022, 323, 111409. [Google Scholar] [CrossRef]
  119. Pauwels, L.; Goossens, A. The JAZ proteins: A crucial interface in the jasmonate signaling cascade. Plant Cell 2011, 23, 3089–3100. [Google Scholar] [CrossRef] [Green Version]
  120. Ghorbel, M.; Brini, F.; Sharma, A.; Landi, M. Role of jasmonic acid in plants: The molecular point of view. Plant Cell Rep. 2021, 40, 1471–1494. [Google Scholar] [CrossRef] [PubMed]
  121. Bari, R.; Jones, J.D. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69, 473–488. [Google Scholar] [CrossRef] [PubMed]
  122. Kumar, S.; Shah, S.H.; Vimala, Y.; Jatav, H.S.; Ahmad, P.; Chen, Y.; Siddique, K.H. Abscisic acid: Metabolism, transport, crosstalk with other plant growth regulators, and its role in heavy metal stress mitigation. Front. Plant Sci. 2022, 13, 972856. [Google Scholar] [CrossRef]
  123. Kiribuchi, K.; Jikumaru, Y.; Kaku, H.; Minami, E.; Hasegawa, M.; Kodama, O.; Seto, H.; Okada, K.; Nojiri, H.; Yamane, H. Involvement of the basic helix-loop-helix transcription factor RERJ1 in wounding and drought stress responses in rice plants. Biosci. Biotechnol. Biochem. 2005, 69, 1042–1044. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  124. Valea, I.; Motegi, A.; Kawamura, N.; Kawamoto, K.; Miyao, A.; Ozawa, R.; Takabayashi, J.; Gomi, K.; Nemoto, K.; Nozawa, A. The rice wound-inducible transcription factor RERJ1 sharing same signal transduction pathway with OsMYC2 is necessary for defense response to herbivory and bacterial blight. Plant Mol. Biol. 2022, 109, 651–666. [Google Scholar] [CrossRef] [PubMed]
  125. Majid, I.; Kumar, A.; Abbas, N. A basic helix loop helix transcription factor, AaMYC2-Like positively regulates artemisinin biosynthesis in Artemisia annua L. Ind. Crops Prod. 2019, 128, 115–125. [Google Scholar] [CrossRef]
  126. Shen, Q.; Huang, H.; Xie, L.; Hao, X.; Kayani, S.-I.; Liu, H.; Qin, W.; Chen, T.; Pan, Q.; Liu, P. Basic Helix-Loop-Helix transcription factors AabHLH2 and AabHLH3 function antagonistically with AaMYC2 and are negative regulators in artemisinin biosynthesis. Front. Plant Sci. 2022, 13, 885622. [Google Scholar] [CrossRef]
  127. Dolferus, R. To grow or not to grow: A stressful decision for plants. Plant Sci. 2014, 229, 247–261. [Google Scholar] [CrossRef] [PubMed]
  128. Gil, K.E.; Park, C.M. Thermal adaptation and plasticity of the plant circadian clock. New Phytol. 2019, 221, 1215–1229. [Google Scholar] [CrossRef] [PubMed]
  129. Raza, A.; Ashraf, F.; Zou, X.; Zhang, X.; Tosif, H. Plant adaptation and tolerance to environmental stresses: Mechanisms and perspectives. In Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I.; Springer: Singapore, 2020; pp. 117–145. [Google Scholar]
  130. Haggag, W.M.; Abouziena, H.; Abd-El-Kreem, F.; El Habbasha, S. Agriculture biotechnology for management of multiple biotic and abiotic environmental stress in crops. J. Chem. Pharm. Res. 2015, 7, 882–889. [Google Scholar]
  131. Wassmann, R.; Jagadish, S.; Heuer, S.; Ismail, A.; Redona, E.; Serraj, R.; Singh, R.; Howell, G.; Pathak, H.; Sumfleth, K. Climate change affecting rice production: The physiological and agronomic basis for possible adaptation strategies. Adv. Agron. 2009, 101, 59–122. [Google Scholar]
  132. Raza, A.; Razzaq, A.; Mehmood, S.S.; Zou, X.; Zhang, X.; Lv, Y.; Xu, J. Impact of climate change on crops adaptation and strategies to tackle its outcome: A review. Plants 2019, 8, 34. [Google Scholar] [CrossRef] [Green Version]
  133. Lee, H.-J.; Seo, P.J. Ca2+ talyzing initial responses to environmental stresses. Trends Plant Sci. 2021, 26, 849–870. [Google Scholar] [CrossRef] [PubMed]
  134. Seo, J.S.; Joo, J.; Kim, M.J.; Kim, Y.K.; Nahm, B.H.; Song, S.I.; Cheong, J.J.; Lee, J.S.; Kim, J.K.; Choi, Y.D. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J. 2011, 65, 907–921. [Google Scholar] [CrossRef] [PubMed]
  135. Teng, Y.; Lv, M.; Zhang, X.; Cai, M.; Chen, T. BEAR1, a bHLH transcription factor, controls salt response genes to regulate rice salt response. J. Plant Biol. 2022, 65, 217–230. [Google Scholar] [CrossRef]
  136. Alam, M.S.; Kong, J.; Tao, R.; Ahmed, T.; Alamin, M.; Alotaibi, S.S.; Abdelsalam, N.R.; Xu, J.-H. CRISPR/Cas9 mediated knockout of the OsbHLH024 transcription factor improves salt stress resistance in rice (Oryza sativa L.). Plants 2022, 11, 1184. [Google Scholar] [CrossRef]
  137. Gu, X.; Gao, S.; Li, J.; Song, P.; Zhang, Q.; Guo, J.; Wang, X.; Han, X.; Wang, X.; Zhu, Y. The bHLH transcription factor regulated gene OsWIH2 is a positive regulator of drought tolerance in rice. Plant Physiol. Biochem. 2021, 169, 269–279. [Google Scholar] [CrossRef]
  138. Liu, J.; Shen, Y.; Cao, H.; He, K.; Chu, Z.; Li, N. OsbHLH057 targets the AATCA cis-element to regulate disease resistance and drought tolerance in rice. Plant Cell Rep. 2022, 41, 1285–1299. [Google Scholar] [CrossRef]
  139. Zhang, H.; Guo, J.; Chen, X.; Zhou, Y.; Pei, Y.; Chen, L.; Lu, M.; Gong, H.; Chen, R. Pepper bHLH transcription factor CabHLH035 contributes to salt tolerance by modulating ion homeostasis and proline biosynthesis. Hortic. Res. 2022, 9, uhac203. [Google Scholar] [CrossRef]
  140. Liang, X.; Li, Y.; Yao, A.; Liu, W.; Yang, T.; Zhao, M.; Zhang, B.; Han, D. Overexpression of MxbHLH18 increased iron and high salinity stress tolerance in Arabidopsis thaliana. Int. J. Mol. Sci. 2022, 23, 8007. [Google Scholar] [CrossRef]
  141. Zuo, Z.F.; Kang, H.G.; Park, M.Y.; Jeong, H.; Sun, H.J.; Song, P.S.; Lee, H.Y. Zoysia japonica MYC type transcription factor ZjICE1 regulates cold tolerance in transgenic Arabidopsis. Plant Sci. 2019, 289, 110254. [Google Scholar] [CrossRef]
  142. Zuo, Z.-F.; Kang, H.-G.; Hong, Q.-C.; Park, M.-Y.; Sun, H.-J.; Kim, J.; Song, P.-S.; Lee, H.-Y. A novel basic helix-loop-helix transcription factor, ZjICE2 from Zoysia japonica confers abiotic stress tolerance to transgenic plants via activating the DREB/CBF regulon and enhancing ROS scavenging. Plant Mol. Biol. 2020, 102, 447–462. [Google Scholar] [CrossRef]
  143. Qiu, J.-R.; Huang, Z.; Xiang, X.-Y.; Xu, W.-X.; Wang, J.-T.; Chen, J.; Song, L.; Xiao, Y.; Li, X.; Ma, J. MfbHLH38, a Myrothamnus flabellifolia bHLH transcription factor, confers tolerance to drought and salinity stresses in Arabidopsis. BMC Plant Biol. 2020, 20, 1–14. [Google Scholar] [CrossRef]
  144. Chen, W.-J.; Wang, X.; Yan, S.; Huang, X.; Yuan, H.-M. The ICE-like transcription factor HbICE2 is involved in jasmonate-regulated cold tolerance in the rubber tree (Hevea brasiliensis). Plant Cell Rep. 2019, 38, 699–714. [Google Scholar] [CrossRef]
  145. Ji, X.; Nie, X.; Liu, Y.; Zheng, L.; Zhao, H.; Zhang, B.; Huo, L.; Wang, Y. A bHLH gene from Tamarix hispida improves abiotic stress tolerance by enhancing osmotic potential and decreasing reactive oxygen species accumulation. Tree Physiol. 2016, 36, 193–207. [Google Scholar]
  146. Vélez-Bermúdez, I.C.; Schmidt, W. How Plants Recalibrate Cellular Iron Homeostasis. Plant Cell Physiol. 2022, 63, 154–162. [Google Scholar] [CrossRef]
  147. Zheng, L.; Ying, Y.; Wang, L.; Wang, F.; Whelan, J.; Shou, H. Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biol. 2010, 10, 166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  148. Wang, W.; Ye, J.; Ma, Y.; Wang, T.; Shou, H.; Zheng, L. OsIRO3 plays an essential role in iron deficiency responses and regulates iron homeostasis in rice. Plants 2020, 9, 1095. [Google Scholar] [CrossRef] [PubMed]
  149. Zhang, H.; Li, Y.; Yao, X.; Liang, G.; Yu, D. Positive regulator of iron homeostasis1, OsPRI1, facilitates iron homeostasis. Plant Physiol. 2017, 175, 543–554. [Google Scholar] [CrossRef] [Green Version]
  150. Kobayashi, T.; Ozu, A.; Kobayashi, S.; An, G.; Jeon, J.-S.; Nishizawa, N.K. OsbHLH058 and OsbHLH059 transcription factors positively regulate iron deficiency responses in rice. Plant Mol. Biol. 2019, 101, 471–486. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  151. Wang, L.; Ying, Y.; Narsai, R.; Ye, L.; Zheng, L.; Tian, J.; Whelan, J.; Shou, H. Identification of OsbHLH133 as a regulator of iron distribution between roots and shoots in Oryza sativa. Plant Cell Environ. 2013, 36, 224–236. [Google Scholar] [CrossRef] [PubMed]
  152. Sun, K.; Wang, H.; Xia, Z. The maize bHLH transcription factor bHLH105 confers manganese tolerance in transgenic tobacco. Plant Sci. 2019, 280, 97–109. [Google Scholar] [CrossRef]
  153. Dong, Y.; Wang, C.; Han, X.; Tang, S.; Liu, S.; Xia, X.; Yin, W. A novel bHLH transcription factor PebHLH35 from Populus euphratica confers drought tolerance through regulating stomatal development, photosynthesis and growth in Arabidopsis. Biochem. Biophys. Res. Commun. 2014, 450, 453–458. [Google Scholar] [CrossRef]
  154. Kashyap, P.; Deswal, R. Two ICE isoforms showing differential transcriptional regulation by cold and hormones participate in Brassica juncea cold stress signaling. Gene 2019, 695, 32–41. [Google Scholar] [CrossRef] [PubMed]
  155. Chander, S.; Almeida, D.M.; Serra, T.S.; Jardim-Messeder, D.; Barros, P.M.; Lourenço, T.F.; Figueiredo, D.D.; Margis-Pinheiro, M.; Costa, J.M.; Oliveira, M.M. OsICE1 transcription factor improves photosynthetic performance and reduces grain losses in rice plants subjected to drought. Environ. Exp. Bot. 2018, 150, 88–98. [Google Scholar] [CrossRef]
  156. Nakamura, J.; Yuasa, T.; Huong, T.T.; Harano, K.; Tanaka, S.; Iwata, T.; Phan, T.; Iwaya, M. Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation. Plant Biotechnol. 2011, 28, 303–309. [Google Scholar] [CrossRef] [Green Version]
  157. Yao, P.; Sun, Z.; Li, C.; Zhao, X.; Li, M.; Deng, R.; Huang, Y.; Zhao, H.; Chen, H.; Wu, Q. Overexpression of Fagopyrum tataricum FtbHLH2 enhances tolerance to cold stress in transgenic Arabidopsis. Plant Physiol. Biochem. 2018, 125, 85–94. [Google Scholar] [CrossRef] [PubMed]
  158. Ogawa, S.; Kawahara-Miki, R.; Miyamoto, K.; Yamane, H.; Nojiri, H.; Tsujii, Y.; Okada, K. OsMYC2 mediates numerous defence-related transcriptional changes via jasmonic acid signalling in rice. Biochem. Biophys. Res. Commun. 2017, 486, 796–803. [Google Scholar] [CrossRef]
  159. Ohno, S.; Hosokawa, M.; Hoshino, A.; Kitamura, Y.; Morita, Y.; Park, K.-I.; Nakashima, A.; Deguchi, A.; Tatsuzawa, F.; Doi, M. A bHLH transcription factor, DvIVS, is involved in regulation of anthocyanin synthesis in dahlia (Dahlia variabilis). J. Exp. Bot. 2011, 62, 5105–5116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  160. Payyavula, R.S.; Singh, R.K.; Navarre, D.A. Transcription factors, sucrose, and sucrose metabolic genes interact to regulate potato phenylpropanoid metabolism. J. Exp. Bot. 2013, 64, 5115–5131. [Google Scholar] [CrossRef]
Ijms 24 01419 g001 550
Figure 1. Phylogenetic analysis of the species based on genome-wide association study of the basic helix-loop-helix (bHLH) family. The total number of bHLH transcription factors identified from the genome of each species are indicated [5,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64].
Figure 1. Phylogenetic analysis of the species based on genome-wide association study of the basic helix-loop-helix (bHLH) family. The total number of bHLH transcription factors identified from the genome of each species are indicated [5,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64].
Ijms 24 01419 g001
Ijms 24 01419 g002 550
Figure 2. Functional classification of basic helix-loop-helix (bHLH) transcription factors in rice. bHLH genes are involved in various physiological processes for growth, metabolism, signaling, and adaptation to environmental stress.
Figure 2. Functional classification of basic helix-loop-helix (bHLH) transcription factors in rice. bHLH genes are involved in various physiological processes for growth, metabolism, signaling, and adaptation to environmental stress.
Ijms 24 01419 g002
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zuo, Z.-F.; Lee, H.-Y.; Kang, H.-G. Basic Helix-Loop-Helix Transcription Factors: Regulators for Plant Growth Development and Abiotic Stress Responses. Int. J. Mol. Sci. 2023, 24, 1419. https://doi.org/10.3390/ijms24021419

AMA Style

Zuo Z-F, Lee H-Y, Kang H-G. Basic Helix-Loop-Helix Transcription Factors: Regulators for Plant Growth Development and Abiotic Stress Responses. International Journal of Molecular Sciences. 2023; 24(2):1419. https://doi.org/10.3390/ijms24021419

Chicago/Turabian Style

Zuo, Zhi-Fang, Hyo-Yeon Lee, and Hong-Gyu Kang. 2023. "Basic Helix-Loop-Helix Transcription Factors: Regulators for Plant Growth Development and Abiotic Stress Responses" International Journal of Molecular Sciences 24, no. 2: 1419. https://doi.org/10.3390/ijms24021419

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop