SBP-box Genes Research Articles

Pepper SBP-box transcription factor, CaSBP13, plays a negatively role in drought response.

The SBP-box gene significantly influences plant growth, development, and stress responses, yet its function in pepper plants during drought stress remains unexplored. Using virus-induced gene silencing and overexpression strategies, we examined the role of CaSBP13 during drought stress in plants. The results revealed that the expression of CaSBP13 can be induced by drought stress. Silencing of CaSBP13 in pepper notably boosted drought resistance, as evident by decreased active oxygen levels. Furthermore, the water loss rate, relative electrical conductivity, malondialdehyde content, and stomatal density were reduced in CaSBP13-silenced plants compared to controls. In contrast, CaSBP13 overexpression in Nicotiana benthamiana decreased drought tolerance with elevated reactive oxygen levels and stomatal density. Additionally, ABA signaling pathway genes (CaPP2C, CaAREB) exhibited reduced expression levels in CaSBP13-silenced plants post drought stress, as compared to control plants. On the contrary, CaPYL9 and CaSNRK2.4 showed heightened expression in CaSBP13-sienced plants under the same conditions. However, a converse trend for NbAREB, NbSNRK2.4, and NbPYL9 was observed post-four day drought in CaSBP13-overexpression plants. These findings suggest that CaSBP13 negatively regulates drought tolerance in pepper, potentially via ROS and ABA signaling pathways.

Genome-Wide Identification and Expression Analysis of the SBP-Box Gene Family in Loquat Fruit Development.

The loquat (Eriobotrya japonica L.) is a special evergreen tree, and its fruit is of high medical and health value as well as having stable market demand around the world. In recent years, research on the accumulation of nutrients in loquat fruit, such as carotenoids, flavonoids, and terpenoids, has become a hotspot. The SBP-box gene family encodes transcription factors involved in plant growth and development. However, there has been no report on the SBP-box gene family in the loquat genome and their functions in carotenoid biosynthesis and fruit ripening. In this study, we identified 28 EjSBP genes in the loquat genome, which were unevenly distributed on 12 chromosomes. We also systematically investigated the phylogenetic relationship, collinearity, gene structure, conserved motifs, and cis-elements of EjSBP proteins. Most EjSBP genes showed high expression in the root, stem, leaf, and inflorescence, while only five EjSBP genes were highly expressed in the fruit. Gene expression analysis revealed eight differentially expressed EjSBP genes between yellow- and white-fleshed fruits, suggesting that the EjSBP genes play important roles in loquat fruit development at the breaker stage. Notably, EjSBP01 and EjSBP19 exhibited completely opposite expression patterns between white- and yellow-fleshed fruits during fruit development, and showed a close relationship with SlCnr involved in carotenoid biosynthesis and fruit ripening, indicating that these two genes may participate in the synthesis and accumulation of carotenoids in loquat fruit. In summary, this study provides comprehensive information about the SBP-box gene family in the loquat, and identified two EjSBP genes as candidates involved in carotenoid synthesis and accumulation during loquat fruit development.

Genome-wide identification and expression analysis of SBP-box gene family reveal their involvement in hormone response and abiotic stresses in Chrysanthemum nankingense.

SQUAMOSA promoter-binding-protein (SBP)-box family proteins are a class of plant-specific transcription factors, and widely regulate the development of floral and leaf morphology in plant growth and involve in environment and hormone signal response. In this study, we isolated and identified 21 non-redundant SBP-box genes in Chrysanthemum nankingense with bioinformatics analysis. Sequence alignments of 21 CnSBP proteins discovered a highly conserved SBP domain including two zinc finger-like structures and a nuclear localization signal region. According to the amino acid sequence alignments, 67 SBP-box genes from Arabidopsis thaliana, rice, Artemisia annua and C. nankingense were clustered into eight groups, and the motif and gene structure analysis also sustained this classification. The gene evolution analysis indicated the CnSBP genes experienced a duplication event about 10 million years ago (Mya), and the CnSBP and AtSPL genes occurred a divergence at 24 Mya. Transcriptome data provided valuable information for tissue-specific expression profiles of the CnSBPs, which highly expressed in floral tissues and differentially expressed in leaf, root and stem organs. Quantitative Real-time Polymerase Chain Reaction data showed expression patterns of the CnSBPs under exogenous hormone and abiotic stress treatments, separately abscisic acid, salicylic acid, gibberellin A3, methyl jasmonate and ethylene spraying as well as salt and drought stresses, indicating that the candidate CnSBP genes showed differentiated spatiotemporal expression patterns in response to hormone and abiotic stresses. Our study provides a systematic genome-wide analysis of the SBP-box gene family in C. nankingense. In general, it provides a fundamental theoretical basis that SBP-box genes may regulate the resistance of stress physiology in chrysanthemum via exogenous hormone pathways.

Identification and Analysis of MADS-box, WRKY, NAC, and SBP-box Transcription Factor Families in Diospyros oleifera Cheng and Their Associations with Sex Differentiation

Transcription factors are crucial for plant growth and development. MADS-box, WRKY, NAC, and SBP-box, some of the most vital transcription factors, are not well identified in Diospyros spp., and their floral development and sex differentiation related functions remain unknown. We identified and analysed 53 MADS-box, 66 WRKY, 83 NAC, and 17 SBP-box transcription factors using the chromosomal D. oleifera genome. There were six DolSBPs identified as miR156 and miR157 targets. According to the multiple sequence alignments of Arabidopsis and D. oleifera proteins and their conserved domains and motifs, DolMADSs were divided into 23 type I and 30 type II. The DolWRKYs, DolNACs, and DolSBPs were divided into 7, 16, and 6 subgroups, respectively. It was found that one DolMADS, five DolWRKYs, one DolNAC, and four DolSBPs may promote unisexual female flowers development, while three DolMADSs, four DolWRKYs, and one DolNAC may enhance unisexual male flowers development. The functions among the different members of the same family may, thus, vary widely. The results will help to elucidate the evolution of the MADS-box, WRKY, NAC, and SBP-box genes families in D. oleifera and to determine their functions in flower development for Diospyros spp.

Genome-Wide Identification and Functional Exploration of SBP-Box Gene Family in Black Pepper (Piper nigrum L.).

Black pepper (Piper nigrum L.), is dubbed “the King of Spices”. However, the lack of genic knowledge has limited the understanding of its physiological processes and hindered the development of its molecular breeding. The SBP-box gene family is an important family in plant development and integrates multiple physiological processes. Here, we made a genome-wide identification of the pepper SBP-box gene family to provide evolutionary and functional information about this conserved transcription factor. In total, 34 SBP genes were identified in pepper. All these pepper SBP genes were clustered into eight groups, and one pepper group was not found in Arabidopsis thaliana. Segment duplications played the most important role in the expansion process of pepper SBP genes, and all these duplications were subjected to purifying selection. Half of pepper SBP genes were found miR156 target sites, and 17 miR156s were predicted. The tissue expression analysis revealed the differential expression of pepper SBP genes. Eleven SBP genes were found in four co-expression networks, and the GO enrichment further provides a functional prediction for pepper SBP genes. This study lays a foundation for further studies of pepper and provides a valuable reference for functional mining of pepper SBP genes.

Genome-Wide Characterization and Expression Analysis of the SBP-Box Gene Family in Sweet Orange (Citrus sinensis).

SBP-box is an important plant-specific transcription factor family and is involved in diverse biological processes. Here, we identified a total of 15 SBP-BOX genes in the important fruit crop sweet orange (Citrus sinensis) and characterized their gene structures, conserved domain and motif, chromosomal location, and cis-acting regulatory elements. SBP genes were classified into four subfamilies based on the amino acid sequence homology, and the classification is equally strongly supported by the gene and protein structures. Our analysis revealed that segmental duplication events were the main driving force in the evolution of CsSBP genes, and gene pairs might undergo extensive purifying selection. Further synteny analysis of the SBP members among sweet orange and other plant species provides valuable information for clarifying the CsSBP family evolutionary relationship. According to publicly available RNA-seq data and qRT-PCR analysis from various sweet orange tissues, CsSBP genes may be expressed in different tissues and developmental stages. Gene expression analysis showed variable expression profiles of CsSBP genes under various abiotic stresses, such as high and low-temperature, salt, and wound treatments, demonstrating the potential role of SBP members in sweet orange response to abiotic stress. Noticeably, all CsSBP genes were also downregulated in sweet orange upon the infection of an important fungal pathogen Diaporthe citri. Our results provide valuable information for exploring the role of SBP-Box in sweet orange.

Identification and Expression Analysis of the SBP-box Gene Family Related to Abiotic Stress in Tea Plant (Camellia sinensis (L.) O. Kuntze)

Identification and Expression Analysis of the SBP-box Gene Family Related to Abiotic Stress in Tea Plant (Camellia sinensis (L.) O. Kuntze)

Identification, evolution, and expression analysis of SBP-box gene family in kiwifruit (Actinidia chinensis Planch.)

Identification, evolution, and expression analysis of SBP-box gene family in kiwifruit (Actinidia chinensis Planch.)

Molecular evolution and genome-wide analysis of the SBP-box family in cucumber (Cucumis sativas)

SQUAMOSA promoter binding protein (SBP)-box gene family encodes a group of transcription factors that play essential roles in plant development and stress responses. However, the SBP-box gene family has not been well characterized in cucumber (Cucumis sativas). In the present study, we identified 15 putative SBP-box genes (CuSBPs) distributing on 4 chromosomes of cucumber. Evolutionary analysis showed that the green plant SBP family originated from liverworts. Phylogenic analysis divided CuSBPs into 6 groups similar to those of Arabidopsis and rice. Intron–exon and motif structure within each group shared common features. Expression pattern analysis of transcriptional data for flowering demonstrated conserved CuSBPs function in vegetative-to-reproductive transition. Gene expression of cucumber leaves in response to powdery mildew showed that conserved CuSBPs function in regulatory pathways such as hormone regulation pathways. Moreover, codon bias analysis explained the mutation and selection pressure exerted on SBP-box genes. This study comprehensively characterized cucumber CuSBP gene family, which is likely to provide a foundation to explore the functions of CuSBPs for improving yield, quality and stress tolerance of cucumber in the future.

Genome-wide identification, characterization, and expression patterns analysis of the SBP-box gene family in wheat (Triticum aestivum L.)

SQUAMOSA promoter-binding protein (SBP)-box genes encode a family of plant-specific transcription factors that play roles in plant growth and development. The characteristics of SBP-box genes in rice (Oryza sativa) and Arabidopsis have been reported, but their potential roles in wheat (Triticum aestivum) are not fully understood. In this study, 48 SBP-box genes (TaSBPs) were identified; they were located in all wheat chromosomes except for 4B and 4D. Six TaSBPs were identified as tandem duplication genes that formed three tandem duplication pairs, while 22 were segmentally duplicated genes that formed 16 segmental duplication pairs. Subcellular localization prediction showed TaSBPs were located in nucleus. Among the 48 TaSBPs, 24 were predicted to be putative targets of TamiR156. Phylogenetic analysis showed that TaSBPs, AtSBPs, and OsSBPs that shared similar functions were clustered into the same subgroups. The phylogenetic relationships between the TaSBPs were supported by the identification of highly conserved motifs and gene structures. Four types of cis-elements––transcription-related, development-related, hormone-related, and abiotic stress-related elements––were found in the TaSBP promoters. Expression profiles indicated most TaSBPs participate in flower development and abiotic stress responses. This study establishes a foundation for further investigation of TaSBP genes and provides novel insights into their biological functions.

Comparative study of the SBP-box gene family in rice siblings

SBP-box genes are a class of plant-specific transcription factors which have a common DNA-binding domain (SBP-domain) with an unusual zinc-finger architecture. Many of the genes in this class are thought to play a developmental role and a few are involved in the determination of plant architecture. We have made a comparative study of these genes in the genomes of rice (Oryza sativa japonica and Oryza sativa indica) and its nine siblings using a recently proposed hybrid method for orthology and paralogy detection (HyPPO). According to HyPPO, the SBP-box proteins of rice siblings could be divided into twenty primary orthologous groups on the basis of their overall sequence features. This contrasts with a much less number of groups found in earlier work with other plant genomes using phylogenetic analysis of the SBP-domains only. The orthologous groups reported by HyPPO showed close correspondence in exon-intron structure and motif conservation. Comparison between different Oryza species revealed disparity in the maintenance of orthologous genes which may result in their different developmental characteristics. Inclusion of the SBP-box proteins from A. thaliana did not result in any change in the orthologous groups except for the A. thaliana proteins being added to some of the existing groups. The closer correspondence between the proteins in the primary orthologous clusters is expected to help in a more reliable prediction of their functions. It is also expected to provide better insight into the evolutionary history of this class of plant-specific proteins.

Differentially expressed miRNAs in anthers may contribute to the fertility of a novel Brassica napus genic male sterile line CN12A

In Brassica napus L. (rapeseed), complete genic male sterility (GMS) plays an important role in the utilization of heterosis. Although microRNAs (miRNAs) play essential regulatory roles during bud development, knowledge of how GMS is regulated by miRNAs in rapeseed is rather limited. In this study, we obtained a novel recessive GMS system, CN12AB. The sterile line CN12A has defects in tapetal differentiation and degradation. Illumina sequencing was employed to examine the expression of miRNAs in the buds of CN12A and the fertile line CN12B. We identified 85 known miRNAs and 120 novel miRNAs that were expressed during rapeseed anther development. When comparing the expression levels of miRNAs between CN12A and CN12B, 19 and 18 known miRNAs were found to be differentially expressed in 0.5–1.0 mm buds and in 2.5–3.0 mm buds, respectively. Among these, the expression levels of 14 miRNAs were higher and the levels of 23 miRNAs were lower in CN12A compared with CN12B. The predicted target genes of these differentially expressed miRNAs encode protein kinases, F-box domain-containing proteins, MADS-box family proteins, SBP-box gene family members, HD-ZIP proteins, floral homeotic protein APETALA 2 (AP2), and nuclear factor Y, subunit A. These targets have previously been reported to be involved in pollen development and male sterility, suggesting that miRNAs might act as regulators of GMS in rapeseed anthers. Furthermore, RT-qPCR data suggest that one of the differentially expressed miRNAs, bna-miR159, plays a role in tapetal differentiation by regulating the expression of transcription factor BnMYB101 and participates in tapetal degradation and influences callose degradation by manipulating the expression of BnA6. These findings contribute to our understanding of the roles of miRNAs during anther development and the occurrence of GMS in rapeseed.

Dynamic Expansion and Functional Evolutionary Profiles of Plant Conservative Gene Family SBP-Box in Twenty Two Flowering Plants and the Origin of miR156.

Conservative gene families in plants, which are closely related to innovations in flowering plants, have long and complex evolutionary histories. Here, we used the SQUAMOSA promoter-binding protein (SBP-box) gene family as an example to study conservative gene families in flowering plants. In total, 11 groups, including nine angiosperm-conservative groups and two monocot- and eudicot-specific groups, were identified. Among the nine angiosperm-conservative groups, four are conserved in all land plants and the remaining five are angiosperm-specific. The five angiosperm-specific groups exhibit structural and functional diversity and evolved together, along with the evolution of flowering plants. The expansion of SBP genes was affected by miR156, and the miR156-regulated SBP genes tend to retain more copies. Our results reflect the dynamic evolutionary process of the different groups, with the identification of two genetic lines via synteny analyses. In addition, miR156 showed a close evolutionary relationship with SBP genes, suggesting that it may originate from face-to-face tandem duplication of SBP genes. SBP genes without an miR156 binding locus are usually functionally conservative or housekeeping like, belonging to the terrestrial-conservative group. In contrast, SBP genes with miR156 binding sites are selected by angiosperms to regulate more complex physiological processes.

Transcription Factor CaSBP12 Negatively Regulates Salt Stress Tolerance in Pepper (Capsicum annuum L.).

SBP-box (Squamosa-promoter binding protein) genes are a type of plant-specific transcription factor and play important roles in plant growth, signal transduction, and stress response. However, little is known about the role of pepper SBP-box transcription factor genes in response to abiotic stress. Here, one of the pepper SBP-box gene, CaSBP12, was selected and isolated from pepper genome database in our previous study. The CaSBP12 gene was induced under salt stress. Silencing the CaSBP12 gene enhanced pepper plant tolerance to salt stress. The accumulation of reactive oxygen species (ROS) of the detached leaves of CaSBP12-silenced plants was significantly lower than that of control plants. Besides, the Na+, malondialdehyde content, and conductivity were significantly increased in control plants than that in the CaSBP12-silenced plants. In addition, the CaSBP12 over-expressed Nicotiana benthamiana plants were more susceptible to salt stress with higher damage severity index percentage and accumulation of ROS as compared to the wild-type. These results indicated that CaSBP12 negatively regulates salt stress tolerance in pepper may relate to ROS signaling cascades.

Molecular characterization of SBP-box gene family during floral induction in walnut (Juglans regia L.)

SQUAMOSA promoter-binding protein (SBP)-box genes regulate plant-specific transcription factors that play vital roles in diverse biological processes. In this study, we identified 48 SBP-box genes from Juglans regia (JrSBPs) based on the transcriptome dataset. Nineteen of these JrSBPs were predicted to be putative target genes of jre-miR156/157. Phylogenetic tree based on the conserved SBP domains divided the JrSBPs into nine groups, analogous to those from Arabidopsis. JrSBP members within the same group shared similar motifs. Cis-elements analysis implied that JrSBP genes were regulated by light, phytohormones, and stresses. Functions of JrSBP genes were predicted and analyzed by comparing the proteins of JrSBPs and SPLs from Arabidopsis. Expression profile of JrSBPs was analyzed based on RNA-seq and RT-qPCR. The results should provide fundamental information for understanding the roles of JrSBPs during floral induction.

Genome-wide analysis of the SBP-box gene family transcription factors and their responses to abiotic stresses in tea (Camellia sinensis)

SQUAMOSA promoter-binding protein (SBP)-box gene family is one kind of plant-specific transcription factor that plays important roles in the process of resisting abiotic stress. The SBP-box gene family has been studied in many species, but their functions are not yet clear in Camellia sinensis var. sinensis (CSS) (tea) plants. In our study, 25 SBP-box genes in the CSS were identified in the reference genome and classified into six groups based on a phylogenetic tree. The expression pattern of CsSBP genes under temperature stresses showed that CsSBPs were involved in the process of resisting temperature stresses. CsSBP8 had a positive effect on the anthocyanin accumulation during high temperature exposures, but CsSBP12 has a high correlation with anthocyanin accumulation during both high and low temperature. This study provides a foundation for the further study of CsSBP genes involved in the anthocyanin biosynthesis pathway during the temperature stress in tea.

Genome-wide identification, phylogeny, and expression analysis of the SBP-box gene family in Euphorbiaceae

BackgroundEuphorbiaceae is one of the largest families of flowering plants. Due to its exceptional growth form diversity and near-cosmopolitan distribution, it has attracted much interest since ancient times. SBP-box (SBP) genes encode plant-specific transcription factors that play critical roles in numerous biological processes, especially flower development. We performed genome-wide identification and characterization of SBP genes from four economically important Euphorbiaceae species.ResultsIn total, 77 SBP genes were identified in four Euphorbiaceae genomes. The SBP proteins were divided into three length ranges and 10 groups. Group-6 was absent in Arabidopsis thaliana but conserved in Euphorbiaceae. Segmental duplication played the most important role in the expansion processes of Euphorbiaceae SBP genes, and all the duplicated genes were subjected to purify selection. In addition, about two-thirds of the Euphorbiaceae SBP genes are potential targets of miR156, and some miR-regulated SBP genes exhibited high intensity expression and differential expression in different tissues. The expression profiles related to different stress treatments demonstrated broad involvement of Euphorbiaceae SBP genes in response to various abiotic factors and hormonal treatments.ConclusionsIn this study, 77 SBP genes were identified in four Euphorbiaceae species, and their phylogenetic relationships, protein physicochemical characteristics, duplication, tissue and stress response expression, and potential roles in Euphorbiaceae development were studied. This study lays a foundation for further studies of Euphorbiaceae SBP genes, providing valuable information for future functional exploration of Euphorbiaceae SBP genes.

OsSPL10, a SBP-Box Gene, Plays a Dual Role in Salt Tolerance and Trichome Formation in Rice (Oryza sativa L.).

Salinity is one of the major abiotic stress factors limiting rice production. Glabrousness is a trait of agronomic importance in rice (Oryza sativa L.). We previously found a single-gene recessive mutant sst, which displayed increased salt tolerance and glabrous leaf and glume without trichomes, and identified an SBP-box gene OsSPL10 as the candidate of the SST gene. In this study, OsSPL10-knockout and OsSPL10-overexpression mutants were created to check the function of the gene. The knockout mutants exhibited enhanced salt tolerance and glabrous leaves and glumes as expected, while the overexpression mutants showed opposite phenotypes, in which both salt sensitivity and trichome density on leaf and glume were increased. These results clearly confirmed that OsSPL10 is SST, and suggested that OsSPL10 controls the initiation rather than the elongation of trichomes. In addition, expression analysis indicated that OsSPL10 was preferentially expressed in young panicle and stem, and protein OsSPL10 was localized in nucleus. Taken together, OsSPL10 negatively controls salt tolerance but positively controls trichome formation in rice.

Genome-wide identification, phylogenetic and expression analysis of SBP-box gene family in barley (Hordeum vulgare L.)

The SQUAMOSA PROMOTER BINDING PROTEIN box (SBP-box) gene family is a unique family of transcription factors in plants, which is found widely in green plants. This family functions involve many aspects of crop genetic improvement, such as yield, floral period, and stress resistances; therefore, it has an important practical application value. In this study, 14 non-redundant SBP-box genes were identified and isolated in barley (Hordeum vulgare L.) using Hordeum vulgare.IBSC_v2 in combination with bioinformatics analysis. The results revealed that 13 of these genes were unevenly distributed on five chromosomes, and another gene has not been anchored yet. Sequence alignments demonstrated that each SBP protein has highly conserved functional elements (zinc finger structure and nuclear localization signal sequence). Gene structure analysis indicated their diversified exon-introns structure. Phylogenetic analysis was used to classify the barley SBP-box genes into five subfamilies (D–H). Each subfamily was found to contain similar protein motifs and gene structures. Expression profiles based on the barley RNA-seq database found that the barley SBP-box gene family expresses the highest amount in the inflorescence and showed different expression patterns in different tissues and different stages. Overall, the results indicated that the barley SBP-box gene family is relatively conserved in evolution and function, and plays a crucial role in many stages of barley plant growth development. Our results provide a theoretical reference for subsequent studies of molecular regulation and genetic breeding of SBP-box family genes in barley growth and development.

Genome-wide identification of the SPL gene family in Tartary Buckwheat (Fagopyrum tataricum) and expression analysis during fruit development stages

BackgroundSPL (SQUAMOSA promoter binding protein-like) is a class of plant-specific transcription factors that play important roles in many growth and developmental processes, including shoot and inflorescence branching, embryonic development, signal transduction, leaf initiation, phase transition, and flower and fruit development. The SPL gene family has been identified and characterized in many species but has not been well studied in tartary buckwheat, which is an important edible and medicinal crop.ResultsIn this study, 24 Fagopyrum tataricum SPL (FtSPL) genes were identified and renamed according to the chromosomal distribution of the FtSPL genes. According to the amino acid sequence of the SBP domain and gene structure, the SPL genes were divided into eight groups (group I to group VII) by phylogenetic tree analysis. A total of 10 motifs were detected in the tartary buckwheat SPL genes. The expression patterns of 23 SPL genes in different tissues and fruits at different developmental stages (green fruit stage, discoloration stage and initial maturity stage) were determined by quantitative real-time polymerase chain reaction (qRT-PCR).ConclusionsThe tartary buckwheat genome contained 24 SPL genes, and most of the genes were expressed in different tissues. qRT-PCR showed that FtSPLs played important roles in the growth and development of tartary buckwheat, and genes that might regulate flower and fruit development were preliminarily identified. This work provides a comprehensive understanding of the SBP-box gene family in tartary buckwheat and lays a significant foundation for further studies on the functional characteristics of FtSPL genes and improvement of tartary buckwheat crops.