Genome-wide Identification of the CIPK Gene Family in Jasmine and Expression Analysis Under Salt Stress

doi:10.21203/rs.3.rs-3339281/v1

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Genome-wide Identification of the CIPK Gene Family in Jasmine and Expression Analysis Under Salt Stress

https://doi.org/10.21203/rs.3.rs-3339281/v1

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Background

Various CIPK genes are involved in abiotic stress responses in plants. Despite the economic importance of jasmine (Jasminum sambac), and the availability of genome data, there are few reports analyzing the CIPK gene family. The aim of this study was to perform a phylogenetic analysis and characterization of the CIPK genes in jasmine.

Results

In the present study, A total of 17 CIPKs were identified, which were unevenly distributed on chromosomes. The JsCIPK protein sequences contained 311–781 amino acids, with a molecular weight of 35.05–87.58 kDa. Phylogenetic analysis revealed that the 17 JsCIPKs could be divided into five classical branches. JsCIPK genes with higher homology showed greater similarity between conserved protein motifs. Collinearity analysis demonstrated that 13 gene pairs in Arabidopsis were collinear with the jasmine sequences. Various hormone-related response- and stress-induced elements were observed in the promoter region of JsCIPK genes. Furthermore, the expression of JsCIPK genes varied in different organs. Finally, the expression analyses of eight JsCIPKs under salt stress were performed.

Conclusions

A systematic analysis of the CIPK gene family in Jasmine and expression analysis under salt stress was provided. These findings lay a foundation for future functional studies of JsCIPKs in jasmine related to growth and development and responses to abiotic stress.

Jasminum sambac

jasmine

CIPK gene family

bioinformatics analysis

phylogenetic relationships

gene structure

Plants are frequently exposed to various abiotic stresses, such as salt, drought, cold, high temperature, and oxidative stress. In response, they have developed complex mechanisms to perceive external signals and adapt to various environmental stimuli through appropriate physiological and morphological changes [1]. For example, in unfavorable environments, plants can maintain a normal metabolic response by upregulating the expression of related genes and changing the structure of certain proteins to maintain the integrity of plant structure and function [2].

When plants respond to exogenous stimuli and biotic and abiotic stresses, intracellular calcium ion (Ca²⁺) levels are regulated [3]. In turn, Ca²⁺ plays a crucial role as a secondary messenger in plant stress signal transduction [4]. Ca²⁺ sensors in plants can be classified into four types: calcin-dependent protein kinases (CDPKs), calmodulins (CaMs), calmodulin-like proteins (CAMLs), and calcineurin B-like proteins (CBLs) [5]. Among them, CBLs are specifically targeted by and interact with the CIPK family of serine/threonine protein kinases, which are unique to plants [6], regulating downstream genes and leading to a range of physiological and biochemical changes [7]. More specifically, CBLs sense changes in Ca²⁺ in plants and combine with CIPK to form a CBL-CIPK complex. This complex binds to the corresponding target proteins, phosphorylates them, and transmits downstream signals, improving the response of plants to stress [8].

CBL-CIPK protein complexes participate in various stress signal transmission networks in plants, such as drought, low temperature, high salt, and low potassium, in response to changes in the expression patterns of CIPK genes in plants [9]. CIPK proteins usually contain a conserved catalytic kinase domain at the N-terminus and a regulatory domain at the C-terminus. The former contains a serine/threonine protein kinase catalytic domain with an activation loop for phosphorylation. The C-terminal regulatory domain consists of the protein phosphatase interaction (PPI) motif and the autoregulatory NAF motif (also known as the FISL motif) [10]. The C-terminal regulatory domain is highly conserved and mediates the interactions between CIPK and CBL proteins [11].

With continuous improvements in genome sequencing technology, CIPK and CBL genes have been widely identified in many species, including Arabidopsis [12], rice [13], maize [6], apple [3], grape [14], pepper [15], rape [16], and tomato [17]. Significant differences in the number of CIPK family members exist among the different plants. Maize, rice, Arabidopsis, and tomato have 43, 31, 26, and 22 CIPK gene family members, respectively. In previous studies, various CBL-CIPK complexes were shown to play an important role in plant responses to abiotic stress and nutrient signaling cascades [14]. Because the sequences and structures of CBLs and CIPKs are highly conserved, scientists have hypothesized that the functions of CBLs and CIPKs are similar within and between species. For example, in Arabidopsis, the salt overly sensitive (SOS) pathway is a well-elucidated salt tolerance pathway [17] and similar SOS signaling networks exist in other species, such as begonia [18], poplar [19], and tomato [17]. Similarly, low temperature, drought, salinity, and other abiotic stresses have been shown to influence the transcription levels of 20 OsCIPKs in rice, among which overexpression of OsCIPK3, OsCIPK12, and OsCIPK15 significantly improved the salt tolerance of transgenic plants, while overexpression of corn ZmCIPK8 significantly improved drought resistance in tobacco (Nicotiana tabacum). Overexpression of wheat (Triticum aestivum) TaCIPK14 enables tobacco to acquire stronger cold adaptation ability [20]. Overexpression of AtCIPK21 in rice can reduce the accumulation of reactive oxygen species in transgenic plants under low-temperature stress [21]. In terms of cold stress, CIPK can induce the expression of Ca²⁺-dependent protein kinases (CPK) and MAPK, and significantly increase the content of polyamines and the activity of antioxidant enzymes in plants. This may be the main way by which CIPK regulates cold resistance in plants.

Jasmine (Jasminum sambac) is a perennial evergreen shrub belonging to the Luteaceae family that can be primarily divided into three types: single-leaved, double-leaved, and multipetaled plants. Jasmine is native to tropical and subtropical India and the Persian Gulf. It has high ornamental, economic, edible, and medicinal value. Most varieties are resistant to cold, drought, frost, wet, and alkaline conditions, and deciduous vines are very cold- and drought-tolerant [22]. The morphology, cultivation management technology, pest control, chemical composition, and extraction of essential oils have been studied in jasmine; however, there are few reports on the bioinformatics analysis of gene families in jasmine (Jasminum sambac). Extensive jasmine genomic data provide an opportunity for genome-wide identification of jasmine, as well as comparative genomic studies.

The aim of this study was to perform a bioinformatics analysis of the CIPK genes in jasmine using bioinformatics tools. Phylogenetic relationships, cis-acting regulatory elements prediction, and functional components were analyzed through comparisons of jasmine genome-wide-identified CIPK homologous sequences. These findings provide a basis for further studies on the biological functions of the CIPK genes in jasmine.

Identification of members of the jasmine CIPK family

The NAF domain (PF03822) and pkinase domain (PF00069) were used as reference sequences. The HMM search method was used to identify potential members of the JsCIPK gene family, and BLASTP was used to search the jasmine protein database using 26 AtCIPKs as query sequences. The results of the two search methods were compiled, redundant sequences were removed from the dataset, and 17 JsCIPK protein sequences were identified. These putative JsCIPK genes were named JsCIPK1–JsCIPK17 according to their locations on different chromosomes. These genes were unevenly distributed on the chromosomes, with only one JsCIPK gene each on chromosomes 8 and 13; two on chromosomes 1, 2, 6, and 11; three on chromosome 9; and four on chromosome 3 (Fig. 1).

Analysis of the physical and chemical properties revealed that the JsCIPK protein sequence ranged from 311 (JsCIPK5) to 781 (JsCIPK1) amino acids (Table 2), with an average amino acid number of 465. The molecular weight (Da) of the proteins ranged from 35049.82 (JsCIPK5) to 87584.34 (JsCIPK1). The theoretical pIs of the CIPKs ranged from 5.52 (JsCIPK10) to 9.24 (JsCIPK6). Analysis of the pI values showed that most of the CIPK proteins were basic; only JsCIPK1 was acidic. The instability indices of JsCIPK2, JsCIPK8, JsCIPK9, JsCIPK10, and JsCIPK17 were > 40, indicating that the proteins may be unstable, whereas the other JsCIPKs were stable. The grand average hydropathicity (GRAVY) was negative, indicating a hydrophilic protein. Subcellular localization showed that all of the proteins were localized to the plasma membrane.

Table 2

Physiological characterization of *JsCIPKs*
Gene Name	Amino acids (no.)	Molecular wt (Da)	Isoelectric points (pH)	Instability Index	GRAVY	Subcellular location prediction
JsCIPK1	781	87584.34	9.2	34.08	-0.3	Plasma membrane
JsCIPK2	466	52539.46	8.83	44.22	-0.293	Plasma membrane
JsCIPK3	427	48192.72	9.12	31.36	-0.292	Plasma membrane
JsCIPK4	439	50258.81	7.14	34.35	-0.438	Plasma membrane
JsCIPK5	311	35049.82	8.14	37.59	-0.251	Plasma membrane
JsCIPK6	427	47803.13	9.24	32.77	-0.336	Plasma membrane
JsCIPK7	431	48451.73	7.25	36.73	-0.162	Plasma membrane
JsCIPK8	453	51333.05	8.7	40.09	-0.333	Plasma membrane
JsCIPK9	423	47904.25	9.13	43.32	-0.261	Plasma membrane
JsCIPK10	413	46984.35	5.52	49.4	-0.387	Plasma membrane
JsCIPK11	448	51180.02	8.95	32.16	-0.372	Plasma membrane
JsCIPK12	445	50465.36	9.09	37.73	-0.324	Plasma membrane
JsCIPK13	546	62336.68	8.68	30.32	-0.462	Plasma membrane
JsCIPK14	423	49621.04	7.63	35.65	-0.462	Plasma membrane
JsCIPK15	442	50283.96	8.91	36.71	-0.415	Plasma membrane
JsCIPK16	492	55492.27	9.18	37.35	-0.28	Plasma membrane
JsCIPK17	523	59268.7	9.04	40.28	-0.274	Plasma membrane

Phylogenetic analysis of the CIPK gene family in jasmine

To study the evolutionary relationship of CIPK proteins between jasmine and Arabidopsis, an ML phylogenetic tree was constructed using the CIPK amino acid sequences. The results showed that the 43 CIPKs could be divided into five subfamilies (named Groups I–V) as follows: Group I, JsCIPK2, JsCIPK3, JsCIPK5, JsCIPK6, JsCIPK13, and JsCIPK15; Group II, JsCIPK9; Goup III, JsCIPK11 and JsCIPK8; Group IV, JsCIPK12; and Group V, JsCIPK1, JsCIPK4, JsCIPK7, JsCIPK10, JsCIPK14, JsCIPK16, and JsCIPK17 (Fig. 2). These results also indicated that intron-rich JsCIPKs clustered into Group V, whereas intron-poor and intron-free JsCIPKs clustered into the other four groups, which was consistent with the results for Arabidopsis.

Gene structure and conserved motifs of JsCIPKs

Structural analysis of JsCIPKs showed that the sequence length of the genes ranged from 1365 bp (JsCIPK9) to 6350 bp (JsCIPK4) and contained coding sequences (CDS) and untranslated region (UTR) with different numbers and lengths, respectively (Fig. 3). UTR statistics showed that JsCIPK2, 3, 5, 6, 9, 11, 12, 13, 15, and 17 had both exon start and end structures. Except for JsCIPK1, all the other members of the gene family contained a complete UTR region. CDS analysis showed that JsCIPK1 and JsCIPK16 contained 16 exons; JsCIPK4, JsCIPK14, and JsCIPK17 contained 14 exons; and JsCIPK7 and JsCIPK10 contained 13 exons, respectively. There were four exons each in JsCIPK5 and JsCIPK13, two in JsCIPK8 and JsCIPK12, and only one in the other JsCIPKs. The CIPK gene family members were divided into intron-harboring and intron-less types, consistent with the results of other plant CIPK gene family members. These results indicated that homologues clustered in the same subfamily have similar genetic structures and conserved functions.

The conserved motifs of the jasmine CIPK protein family were analyzed using the MEME tool, and 10 motifs were predicted. The results showed that the motifs of most JsCIPK proteins were the same in type and sequence, and the higher the homology, the higher the similarity of the motifs. Among them, JsCIPK5 lacked motif 4–7, and JsCIPK10 lacked motif 5 (Fig. 3). A Batch CD-search was used to analyze the CIPK domains of jasmine. The predicted results showed the presence of the CIPK_C domain in the C-terminus of JsCIPKs protein sequences, whereas the PKc_like superfamily was present in the N-terminus of JsCIPKs protein sequence STKc_SnRK3, which had two different domains. The structure of the N-terminal kinase, the base of non-ferferent-1 (SNF-1) kinase, is similar to that of sucrose and matches the structural characteristics of the CIPK protein (Fig. 3). In this study, JsCIPK protein sequences were homologous, and all JsCIPKs clustered into five groups, I–V, according to the type and sequence of the motifs. We speculated that homologous proteins were more similar in the same group, and that there might be functional redundancy.

Collinearity analysis of jasmine CIPK gene family

To further understand the phylogenetic relationship of CIPKs, a collinearity analysis diagram of Arabidopsis and J. japonicum genes, and a collinearity diagram of CIPK gene family members of each species were constructed. The results showed that 13 gene pairs in Arabidopsis were collinear with jasmine genes (Fig. 4a). A collinear relationship was observed, including among JsCIPK15, AtCIPK12, AtCIPK13, ATCIPK18, ATCIPK19, JsCIPK2, AtCIPK12, AtCIPK13 and ATCIPK19; JsCIPK6 with AtCIPK1 and AtCIPK17; JsCIPK9 with AtCIPK4 and AtCIPK7; and JsCIPK12 with AtCIPK14 and AtCIPK22. The collinearity pairs of Arabidopsis and jasmine included JsCIPK3 and AtCIPK22; JsCIPK4 and AtCIPK3; JsCIPK13 and AtCIPK15; JsCIPK16 and AtCIPK23; and JsCIPK17 and AtCIPK21. In addition, the CIPKs of J. japonicum included four gene replication pairs: JsCIPK1:JsCIPK16, JsCIPK2:JsCIPK15, and JsCIPK3:JsCIPK14 (Fig. 4b).

Analysis of cis-acting elements of CIPK gene family members in jasmine

To explore the potential functions of CIPK genes, cis-acting element prediction was performed on the promoter region sequence 2000 bp upstream of the JsCIPK start site (Fig. 5). The results demonstrated that there were several cis-acting elements in the promoter region, and the types and quantities of cis-acting elements differed in different gene members. Eight components were identified in the promoter region of CIPK, including ABRE, TGA-element, TC-rich, GARE-motif, LRE, LTR, MeJA, and SA. Except for JsCIPK4, all of the other genes contained more than four types of functional elements. All of the JsCIPKs contained light-response elements, most of which contained methyl jasmine- and abscisic acid-response elements. Among these, 14 genes had abscisic acid cis-acting elements, 13 had methyl jasmine cis-acting elements, and most had low-temperature-, salicylic acid-, and gibberellin-response elements. Three gene family members had auxin-response elements and three had defense stress elements, suggesting that the three family members with defense stress elements might be involved in the abiotic stress response in jasmine.

Expression analysis of JsCIPK genes

Heat map analysis revealed that JsCIPK5 was not expressed in any organ. JsCIPK1, JsCIPK2, JsCIPK6, and JsCIPK13 were strongly expressed in leaves; and JsCIPK1, JsCIPK2, and JsCIPK13 were highly expressed in flowers. JsCIPK2 and JsCIPK12 were significantly expressed in roots, whereas JsCIPK1, JsCIPK6, and JsCIPK13 were expressed in stems. The expression of JsCIPK2 in roots was higher than that in the leaves and flowers, and the expression of JsCIPK2 was relatively high in all tissues. Other JsCIPK genes were expressed at low levels in all tissues. Based on these results, the expression of most JsCIPK genes appeared to be tissue-specific (Fig. 6).

To determine the role of JsCIPKs on the response to salt stress, the expression of eight JsCIPKs were analyzed (Fig. 7). The results demonstrated that the expression of all Js CIPKs had varying degrees of response under salt stress. It is worth mentioning that the expression of JsCIPK6 was down-regulated by salt stress at different time, and the expression of JsCIPK8 was up-regulated significately.

The CIPK gene participates in plant development in Arabidopsis and rice (Kanwar et al., 2014); however, there are no corresponding reports in jasmine. In this study, 17 CIPK gene family members were screened through bioinformatics analysis, and all of these genes were comprehensively identified, including analysis of their evolutionary relationship, chromosome structure, and chromosome distribution.

The first plant CIPK was discovered in the model plant Arabidopsis in which 26 CIPKs have now been identified [23]. In addition, among Solanaceae plants, 15 CIPKs have been identified in eggplant [24] and 21 in pepper. Among the Gramineae, 34 CIPKs have been identified in rice [25], 51 in turnip [26], and 43 in maize [27]. Among woody plants, 16 CIPKs have been identified in plum and 20 in grapes [14]. CIPKs have also been detected in algae, mosses, ferns, Cucurbitaceae, and other plants. Analysis of the location of CIPKs on chromosomes showed that the number of CIPKs distributed on chromosomes 3, 6, and 9 was higher than that on other chromosomes, which is consistent with millet and maize in the Gramineae. The uneven distribution of CIPKs may be related to species evolution and genetic variation.

NAF- and PPI-conserved motifs mediate specific binding of CBL-CIPK and PP2C-CIPK signal transduction pathways, respectively. In this study, a motif5 deletion was observed in the gene structure of JsCIPK5 and JsCIPK10. However, whether deletion of this motif affects the signaling pathway of CIPK remains to be verified. A Batch CD-search revealed that all JsCIPKs were composed of a highly conserved kinase domain and a relatively conserved regulatory domain, reflecting the highly conserved evolutionary characteristics of JsCIPKs in jasmine.

Analysis of gene expression profiling data showed that the majority of Group I JsCIPKs had significantly higher expression levels in different organs than that of other JsCIPK gene group members. However, a few members of Groups II and III also showed high expression. Subsequently, eight JsCIPKs with high expression levels in different organs were selected as the expression determination under salt stress. The results showed that most JsCIPKs were up-regulated under salt stress, and the expression level reached its highest after 1 h of salt stress treatment. It is worth mentioning that the expression of JsCIPK6 was down-regulated by salt stress at different time, and the expression of JsCIPK8 was up-regulated significately.

In conclusion, 17 JsCIPK genes were identified in this study, and a comprehensive bioinformatics analysis was carried out to determine gene structure, physicochemical properties, chromosomal location, expression patterns in different tissues, and collinearity. Previous studies have shown that CIPKs are involved in various abiotic stress responses, including to drought, low temperature, high pH, and high salinity. The expression levels of JsCIPK2 and JsCIPK13 were very high in in jasmine roots, stems, leaves, and flowers, indicating that these two genes are important in the four major plant growth organs. In contrast, the expression of JsCIPK6 was relatively high in leaves and stems, but low in flowers and roots, thus indicating that this gene is mainly involved in leaf and stem development. Besides, the expression of JsCIPK6 and JsCIPK8 was significately down-regulated and up-regulated by salt treatment, respectively. The functions of these two genes in response to salt stress can be further studied in the future. These findings can lay the foundation for the genetic improvement of JsCIPKs in salt tolerant jasmine germplasm.

Identification and characterization of CIPK family members in jasmine

The 26 CIPK protein sequences of Arabidopsis were obtained from the TAIR website and downloaded locally. Three steps were performed to identify the members of the CIPK family in jasmine. First, the Hidden Markov Models (HMM) of Pkinase (PF00069) and NAF (PF03822) were downloaded from the Pfam database, and the protein database (E-value < 0.01) was searched using HMMER3 software [28]. The Arabidopsis CIPK protein sequences were used as seed sequences, and the jasmine protein sequences annotated using BLAST in the jasmine genomic database (https://github.com/maypoleflyn/Jasminum-sambac-genome) were downloaded to the local site for further analysis. If each CIPK member contained multiple genes with high homology, only the sequences with the highest homology were selected. To obtain all CIPKs encoded in the genome, the protein sequences of Jasmine CIPKs (JsCIPKs) were reverse translated into nucleotide sequences and further compared with the nucleotide sequences of the J. sambac genome to avoid missing any unannotated CIPK genes. Further comparative analysis was carried out using a conservative domain database (CCD) [29]. Eventually 17 jasmine CIPK genes were identified. The above results were analyzed using TBtools software. The number of amino acids, isoelectric point (pI), protein stability, and molecular weight of the JsCIPKs were analyzed using the ExPASy website [30]; and secondary structure prediction and subcellular localization was carried out using Subcellular Localization Predictor [31].

Phylogenetic analysis and chromosomal mapping of JsCIPKs

The protein coding sequences of 26 AtCIPK and 17 JsCIPK genes were analyzed by multiple sequence alignment using Clustal X software. After sequence alignment, the matrix was used for phylogenetic tree analysis, and a phylogenetic tree was constructed using the Maximum Likelihood (ML) method in MEGA7 software (Arizona State University, Tempe, AZ, USA), with a bootstrap test value set at 1000 [32]. We extracted the chromosomal location data of the JsCIPK gene family members from genome annotation files and determined whole chromosome densities. TBtools was used for visual analysis, showing only those chromosomes containing JsCIPK members [33].

Analysis of conserved motifs and domains of the jasmine CIPK family

Gene sequences were analyzed for gene structure, conserved motifs, conserved structural domains, and multiple sequence alignment. Clustal X was used for multiple sequence alignment analysis of the protein sequences encoded by the 26 AtCIPK and 17 JsCIPK genes. The conserved protein motifs of JsCIPKs were analyzed using online prediction in MEME [34]. Promoter element prediction was performed using the PLANTCARE database [35]. Gene structure, conserved motifs, and cis-acting elements of all members of the CIPK gene family were visualized using the gene structure viewer in TB tools.

Analysis of CIPK gene distribution and collinearity in jasmine

Based on the gene position number, the corresponding chromosomal location information of jasmine was extracted from the genome annotation files [36], visualized, and identified using MapChart software. Analysis of the colinear relationship between gene family members was performed by MCScanX [37].

Prediction of cis-acting elements in the jasmine CIPK gene

The conserved CIPK motif was analyzed using the MEME suite [38]. The Amazing Optional Gene Viewer in TBtools was used to determine the structure of JsCIPK. The cis-elements of all promoter sequences (approximately 2000 bp) were identified using PlantCARE [36].

Analysis of the expression patterns of CIPK genes in jasmine

RNA-seq data of jasmine root, stem, leaf, and flower organs were obtained from the NCBI SRA database under accession number SRR14317414-SRR14317417. Then the expression levels of 17 JsCIPK genes were collected and analyzed, and a heat map was generated using TBTools.

Expression analysis of JsCIPK genes under salt stress

3-month-old jasmine were treated with 300 mM NaCl, and leaves were collected at 0, 1, 6, and 12 h for the expression analysis of JsCIPK genes by qRT-PCR analysis with specific primers (Table 1). Three biological replicates were performed for all treatments. Then, 2−∆∆ CT method was taken as the analyzation of data.

calcin-dependent protein kinases: CDPKs; calmodulins: CaMs; calmodulin-like proteins: CAMLs; calcineurin B-like proteins: CBLs; the protein phosphatase interaction: PPI; salt overly sensitive: SOS; Ca²⁺-dependent protein kinases: CPK; contained coding sequences: CDS; non-ferferent-1: SNF-1; qRT-PCR: Quantitative real-time PCR

Acknowledgments
Not applicable.

Authors’ contributions

RW and LY conceived and designed the study. LY, RW, KC, TC, XH and XZ conducted the experiments and analyzed the data. LY and RW wrote the manuscript. All authors reviewed the manuscript.

Funding

This work was supported by the [Handan Science and Technology Research and Development Plan Project] under Grant [number 21422012321]; and [General Project of the Natural Science Foundation of Hebei Province] under Grant [number C2022402006].

Data availability statement

The jasmine genome, annotation file, and RNA-seq data were deposited in Github (https://github.com/maypoleflyn/Jasminum-sambac-genome).

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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No competing interests reported.

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Genome-wide Identification of the CIPK Gene Family in Jasmine and Expression Analysis Under Salt Stress

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Abstract

Background

Results

Conclusions

Figures

Background

Results

Identification of members of the jasmine CIPK family

Phylogenetic analysis of the CIPK gene family in jasmine

Gene structure and conserved motifs of JsCIPKs

Collinearity analysis of jasmine CIPK gene family

Analysis of cis-acting elements of CIPK gene family members in jasmine

Expression analysis of JsCIPK genes

Discussion

Methods

Identification and characterization of CIPK family members in jasmine

Phylogenetic analysis and chromosomal mapping of JsCIPKs

Analysis of conserved motifs and domains of the jasmine CIPK family

Analysis of CIPK gene distribution and collinearity in jasmine

Prediction of cis-acting elements in the jasmine CIPK gene

Analysis of the expression patterns of CIPK genes in jasmine

Expression analysis of JsCIPK genes under salt stress

Abbreviations

Declarations

References

Additional Declarations

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