Skip to main content
Download PDF

Identification and characteristics of SnRK genes and cold stress-induced expression profiles in Liriodendron chinense

BMC Genomics volume 23, Article number: 708 (2022) Cite this article

Abstract

Background

The sucrose non-fermenting 1 (SNF1)-related protein kinases (SnRKs) play a vivid role in regulating plant metabolism and stress response, providing a pathway for regulation between metabolism and stress signals. Conducting identification and stress response studies on SnRKs in plants contributes to the development of strategies for tree species that are more tolerant to stress conditions.

Results

In the present study, a total of 30 LcSnRKs were identified in Liriodendron chinense (L. chinense) genome, which was distributed across 15 chromosomes and 4 scaffolds. It could be divided into three subfamilies: SnRK1, SnRK2, and SnRK3 based on phylogenetic analysis and domain types. The LcSnRK of the three subfamilies shared the same Ser/Thr kinase structure in gene structure and motif composition, while the functional domains, except for the kinase domain, showed significant differences. A total of 13 collinear gene pairs were detected in L. chinense and Arabidopsis thaliana (A. thaliana), and 18 pairs were detected in L. chinense and rice, suggesting that the LcSnRK family genes may be evolutionarily more closely related to rice. Cis-regulation element analysis showed that LcSnRKs were LTR and TC-rich, which could respond to different environmental stresses. Furthermore, the expression patterns of LcSnRKs are different at different times under low-temperature stress. LcSnRK1s expression tended to be down-regulated under low-temperature stress. The expression of LcSnRK2s tended to be up-regulated under low-temperature stress. The expression trend of LcSnRK3s under low-temperature stress was mainly up-or down-regulated.

Conclusion

The results of this study will provide valuable information for the functional identification of the LcSnRK gene in the future.

Peer Review reports

Background

Abiotic stress features a genuine effect on plant development and improvement. Plants have evolved complex and precise signal transduction components because of various misfortunes. As major components of the intracellular signal transduction system, protein kinases play a critical part in the stress response. Among them, sucrose non-fermenting 1 (SNF1)-related protein kinase (SnRK) is broadly included in different physiological life forms [1,2,3,4].

SnRK is a serine/threonine protein kinase whose protein has a conserved Ser/Thr protein kinase domain at the N- terminal. Based on phylogenetic analysis of functional domains, the SnRK family in plants has been divided into three subfamilies: SnRK1, SnRK2, and SnRK3 [5]. The SnRK1 subfamily includes three domains: kinase domain, UBA domain, and KA1 domain. The UBA domain can mediate the non-covalent interactions of the ubiquitination protein [6]. The KA1 domain can interact with a phosphatase upstream of SnRK1 and other proteins [7,8,9]. The SnRK2 and SnRK3 subfamilies are plant-specific proteins that have been impressively extended in embryonic plants [10]. An extremely conserved kinase domain was contained in the N-terminal of SnRK2s, and an acidic amino acid fragments domain was contained in the C-terminal of SnRK2s [11]. The C-terminal domain comprises two sub-domains, Domain I and Domain II. Domain I is a feature of all members of the SnRK2 subfamily and must be activated by osmotic stress. Domain II is only specific for ABA-dependent SnRK2s and can eventually respond to ABA [12, 13]. SnRK3 is also known as Calcineurin B-like protein-interacting protein kinases (CIPK) as it can bind to CBL to participate in the Ca2+ mediated stress response. Besides a kinase-conservative domain at the N- terminal, CIPK also had a specific NAF domain that could mediate CBL binding and a PPI-conservative domain that could mediate PP2C binding at the C- terminal [14, 15]. It was concluded that SnRK2 and SnRK3 were imitated from SnRK1 [16] and rapidly extended and separated with plant advancement, taking an interest in the interaction of metabolic direction and stress response signaling pathways, thus conferring multiple effects on terrestrial plants corresponding to the stimulation to the external environment [17].

The plant SnRK family is widely involved in metabolic regulation, plant growth and progress, and abiotic stress response. SnRK1 is the main regulator of cellular energy homeostasis, which is primarily involved in metabolic regulation and affects plant development. SnRK1 can phosphorylate its downstream target, bZIP63, and activate the cytoplasmic pyruvate phosphokinase (cyPPDK) promoter, thereby coordinating the metabolic and developmental mechanisms of A. thaliana seedling [18]. A. thaliana SnRK1 (AtSnRK1) phosphorylates a bZIP63 transcription factor that binds directly to the ARF19 promoter and activates it, thereby regulating lateral root (LR) formation [19]. Among the three SnRK1 genes in A. thaliana, KIN10 (SNF1 kinase homolog 10)/SnRK1.1 and KIN11 (SNF1 kinase homolog 11)/SnRK1.2 play an imperative role since the expression of KIN12/SnRK1.3 cannot be detected in most tissues [20]. Of these, the KIN10 protein can interact with the stomatal development core transcription factor SPEECHLESS (SPCH) and phosphorylate SPCH to improve the protein stability of SPCH and thus promote stomatal development [21]. The protein encoded by members of the SnRK2 subfamily is a monomeric kinase that regulates plant response to various abiotic stresses. Most SnRK2 can be activated by hypertonic stress, except AtSnRK2.9 [12, 22]. SnRK2-PYR/PYL/RCARs-PP2C is the core pathway for plant response to ABA [23]. During the process, the SnRK2 in plants is switched from a quiescent dephosphorylated state to an activated state that is the center reaction of plants response to ABA and natural stresses. Studies revealed that in A. thaliana, the protein kinase of the B2/3 subset of RAF might phosphorylate and induce SnRK 2.2/2.3/2.6. The protein kinase of the B4 subgroup of RAF might phosphorylate and activate the other 6 ABA-independent SnRK2. It reveals the central part of the RAF-SnRK2 cascade pathway in osmotic stress and ABA signaling [2, 3, 24]. ABA-PYL-PP2C is responsible for inhibiting SnRK2 binding release, while RAF mediates SnRK2 self-activation through phosphorylation, thus initiating SnRK activation [4]. AtSnRK2 protein kinase could be activated by drought and ABA treatment and phosphorylate sucrose transport proteins SWEET11 and SWEET12, thereby promoting root growth under drought stress, improving root-shoot ratio, and drought resistance [25]. As part of the calcium signaling pathway, SnRK3 mediates plant development and responses to ionic and nutritional stress such as high sodium levels, potassium deficiency, and nitrogen starvation [5, 26]. When the plant was under high salinity, the generated calcium signal was sensed by SOS3 (AtCBL4) on the cell membrane. Then SOS3 is combined with SOS2 (AtCIPK24) to form a complex that phosphorylates SOS1 (Na+/H+ antiporter) and removes the excess Na + from the root cells [27, 28]. The CBL1/9-CIPK23 complex could enhance the absorption of environmental potassium by plant cells by activating the potassium channel AKT1 [29, 30] and the plasma membrane potassium transporter HAK5 [31, 32]. In vitro recombination experiments showed that the CBL2/3-CIPK3/9/23/26 fractions efficiently triggered the activity of TPK1/ 3/ 5, which depended on the cytoplasmic calcium concentration [33]. MdCIPK13 and MdCIPK22 improve salt and drought tolerance by targeting the phosphorylated sucrose transporter MdSUT2.2 in apples [27, 34]. Overexpression of BnCBL1-BnCIPK6 in Brassica napus enhances tolerance to high salinity and low potassium [35]. In addition, CIPK14 also regulates the glucose response and interacts with KIN10/SnRK1.1 and KIN11/SnRK1.2 in A. thaliana [36]. Furthermore, the upstream activated kinases of SnRK1, SnAK1/GRIK1, and SnAK2/GRIK2 phosphorylate and activate SOS2 under salt stress [37]. These results indicate an interaction between members of the SnRK subfamily, which plays a role in plant physiological processes besides their important role in responding to high salinity and drought stress. However, the representation of SnRK family members involved in low-temperature stress response needs further investigation.

As plant genomes are increasingly sequenced and analyzed, the plant SnRK protein kinase family has received ceaseless recognition. Its auxiliary properties and expression profiles in response to natural stresses such as salt, drought, and ABA have been explained [38,39,40]. In this study, members of the L. chinense SnRK (LcSnRK) protein kinase family were analyzed for their structural properties and expression profiles under low-temperature stress. It is grown in southern china and is a vital ornamental species [41]. The low-temperature response genes of Liriodendron are expected to be tapped to provide genetic resources and theoretical foundations for the future improvement of Liriodendron germplasm through genetic engineering.

Results

Documentation and physicochemical properties analysis of LcSnRK

In this study, 30 members of LcSnRKs were identified (Additional file 1: Table S1). Three members of LcSnRKs were categorized into the LcSnRK1 subfamily by Pfam analysis. All delimited the kinase-associated domain KA1 (PF02149), except for two members of LcSnRK1s, which also contained the ubiquitin-related domain (UBA) (PF00627). Therefore, we can further subdivide the members of the LcSnRK1 subfamily without the conservative domain of UBA into SnRK1-A; Members of the LcSnRK1 subfamily with the conservative domain of UBA have been classified as LcSnRK1-B (Fig. 1A). Six LcSnRKs were allocated to the SnRK2 subfamily based on the assessment of the conserved domain I, which is approximately 30 amino acids distant from the kinase domain, except for three members of LcSnRK2s that also contained the domain II. Therefore, we can further subdivide the LcSnRK2 subfamily into SnRK2-A and SnRK2-B according to the presence or absence of domain II. Twenty-one LcSnRKs belong to SnRK3/CIPK subfamily, containing the NAF domain (PF03822). This domain comprises 24 amino acids, which can be combined with CBLs. Based on the conventional domain and its arrangement on the chromosome, 30 members of LcSnRKs have been named LcSnRK1.1 ~ LcSnRK1.3, LcSnRK2.1 ~ LcSnRK2.6， LcSnRK3.1 ~ LcSnRK3.21. The amino acid number distribution of proteins from LcSnRK1s, LcSnRK2s, and LcSnRK3s ranged between 519 ~ 547aa, 265 ~ 355aa, 356 ~ 629aa, respectively. The molecular weight ranges of the proteins of LcSnRK1s, LcSnRK2s, and LcSnRK3s were 58.36 ~ 62.44 kDa, 29.77 ~ 40.95 kDa, and 39.95 ~ 70.77 kDa, respectively.

Fig. 1
figure 1

Conserved domains of SnRKs and their phylogenetic relationship. A Distribution of conserved domains in three subfamilies of SnRK. B Phylogenetic tree of SnRK. Green, red, and blue fonts represent members of the AtSnRK, OsSnRK, and LcSnRK families, respectively. Background yellow, blue, and red areas represent SnRK subfamilies 1, 2, and 3, respectively

Full size image

Of the average length and molecular weight of the proteins within the three LcSnRK subfamilies, the amino acid number (537.7 aa) and molecular weight (61.08 kDa) of LcSnRK1s were the largest, while the amino acid number (301.17 aa) and the molecular weight (34.15 kDa) of LcSnRK2s were the smallest.

According to the analysis of the instability index (I.I.), the proteins of LcSnRK1s were predicted to be unstable; half of the proteins of LcSnRK2s (LcSnRK2.2/2.3/2.6) were stable; however, most proteins of the LcSnRK3s were stable (among them, only the four proteins of LcSnRK3.8/3.9/3.18/3.19 were unstable). Except for the predicted signal peptide in LcSnRK 3.21 (the signal peptide cleavage site is within amino acids 1–25), most LcSnRK proteins lacked the signal peptide. Subcellular localization prediction suggested that all LcSnRKs proteins were localized in the nucleus (Additional file 1: Table S1).

Phylogenetic relationship of SnRK gene family

To investigate the systemic diversity relationship among altered subfamilies and members of LcSnRK, an NJ phylogenetic tree was generated based on L. chinense SnRK protein sequences. It was initiated that LcSnRK was divided into three subfamilies, LcSnRK1, LcSnRK2, and LcSnRK3 (Additional file 2: Fig. S1). Phylogenetic trees constructed using the SnRK family proteins from three species, A. thaliana, rice, and L. chinense, exhibited a similar number of members in the SnRK1s (three to four) and the SnRK2s (six to ten) that were present in L. chinense, as well as A. thaliana and rice. Details of the SnRK gene family for rice and A. thaliana are presented in Additional file 3: Table S2. Conversely, the number of members of SnRK3s varies by species. For example, 26 are found in A. thaliana, 34 in rice, and 21 in L. chinense (Fig. 1B).

On the phylogenetic tree, the SnRK genes of each group were distributed equally. Members of the rice SnRK family cluster in the evolutionary branches of the phylogenetic trees outer group. The SnRK1 subfamily has many similarities among its members. Among them, three species had bootstrap scores greater than 50, which may reflect the conservative evolutionary position of LcSnRK1. The bootstrap values of the branches in the SnRK2 and SnRK3 subfamilies are not all greater than 50. Especially in the SnRK2 subfamily where LcSnRK2.4 and AtSnRK2.4 cluster on the same branch; LcSnRK2.1/2.2/2.3 and AtSnRK2.7/2.8 were clustered on the same evolutionary branch; LcSnRK2.5/2.6 and AtSRK2.2/2.3/2.6 were clustered on the same branch.

Examination of the gene structure and conserved motif of LcSnRKs

To explore the development of preparing the SnRK family in L. chinense, the moderated themes of 30 individuals from the LcSnRK family were analyzed in this consideration (Additional file 4: Fig. S2). Dissimilar subfamilies were found to share common features in motif composition and significant differences (Fig. 2A, B). Motifs 1, 4, and 7 encode a pkinase domain in all LcSnRK genes. Motif 14 only exists in the LcSnRK1 and LcSnRK2 families. Motif 12 is presented in all members except SnRK1-A. Motif 12 in SnRK1-B is arranged at the N-terminal. The arrangement pattern of motifs 12, 5, and 14 only exists in the SnRK2 subfamily. Motifs 10, 11, and 8 encode the NAF conservative domain, so these three motifs only exist in the SnRK3 subfamily. In addition, members of the same subfamily shared similar features in the exon-intron structures of the LcSnRK family genes (Fig. 2A, C). LcSnRK1s contain 10 to 11 introns; LcSnRK2s contain 6 to 9 introns. In contrast, the number of introns varies in the LcSnRK3 subfamily, with 13 members containing three or fewer introns and 8 members containing over 10 introns, which differ from the other two subfamilies. Therefore, LcSnRK3 could be divided into two subgroups according to the number of introns, an intron-rich subgroup, and an intron-deficient subgroup. The characteristics of the number of introns suggest that genes in the SnRK1 and SnRK2 subfamilies are structurally more conservative than genes in the LcSnRK3 subfamily.

Fig. 2
figure 2

Conservative motif and exon-intron pattern of LcSnRKs. A Phylogenetic trees of three subfamilies of LcSnRKs. B Conservative motifs of three subfamilies of LcSnRKs. C An exon-intron pattern of three subfamilies of LcSnRKs

Full size image

Cis-regulation element of LcSnRKs

Considering that the SnRK gene family plays a critical part in many natural forms, the promoter of the LcSnRK gene was analyzed in this study to recognize potential administrative components. Hence, giving clues for a more profound understanding of quality control and its reactions provides distinctive boosts. We analyzed the cis-regulatory elements (CREs) on 2 kb of the putative promoters of the LcSnRK gene family members. The detailed distribution of each cis-acting element in the promoter region is presented in Additional file 5: Fig. S3. Here, we grouped the CREs according to response to abiotic and biotic stresses, response to phytohormones, and plant growth and development. The heatmap indicates whether the various elements are over- or under-represented relative to 30 members of the LcSnRK family (Fig. 3). G-Box and ABRE are the most widely distributed, and LcSnRK2.2 has the most G-Box and ABRE elements. In the LcSnRK1 subfamily and the LcSnRK2 subfamily, most members (LcSnRK1.2/1.3/2.1/2.2/2.4/2.5) have more G-Box and ABRE elements (over six). Only four members of the LcSnRK3 subfamily (LcSnRK3.5/3.8/3.15/3.18) had more G-Box and ABRE elements. The 12 LcSnRK genes contained LTR, a cis-acting element associated with a low temperature. LcSnRK3.1 contained three LTRs, and the LcSnRK1 subfamily contained no low-temperature responsive elements. Jasmonates (JA) are involved in various aspects of plant development and are part of the growth-defense trade-off. The 22 LcSnRK genes contained methyl jasmonate-related regulatory elements, including the CGTCA-motif and TGACG-motif. LcSnRK2.5 and LcSnRK3.11 contained most of the CGTCA- and TGACG-motif elements, which are over-represented on the LcSnRK promoters.

Fig. 3
figure 3

Typical cis-regulation element analysis of LcSnRKs

Full size image

Chromosomal location, genomic collinearity, and gene duplication analysis of LcSnRKs

Twenty-five members of the 30 LcSnRK genes were distributed across 16 chromosomes, and 5 genes (LcSnRK1.3, LcSnRK3.18, LcSnRK3.19, LcSnRK3.20, LcSnRK3.21) were mapped to non-assembled genomic fragments (Fig. 4). The positions of the LcSnRK family genes on the chromosomes were relatively dispersed. Four LcSnRK3 subfamily groups have been arranged into clusters on various chromosomes, including LcSnRK3.6/LcSnRK3.7, LcSnRK3.11/LcSnRK3.12, LcSnRK3.15/LcSnRK3.16, and LcSnRK3.18/LcSnRK3.19. These four gene clusters are called tandem duplicates, in which the two 200 bp fragments produced by duplication are within the same chromosome. The term “segment duplication” refers to the occurrence of two duplicate gene pairs in which fragments are on different chromosomes or are dispersed far apart on the same chromosome [42]. Based on BLAST and MCScanX, 10 segment duplication events were identified in this study, and all occurred between different chromosomes (Fig. 5A). This result demonstrated that segment duplication occasions are vital in enhancing the LcSnRK gene. No duplication events were observed within the LcSnRK1 subfamily, affirming the elevated level of preservation within the LcSnRK1 subfamily.

Fig. 4
figure 4

Chromosomal distributions of LcSnRKs. Gene density is shown on each chromosome. The members of LcSnRK1 subfamily are represented in red, the members of LcSnRK2 subfamily in green, and the LcSnRK3 subfamily in blue

Full size image
Fig. 5
figure 5

A Segment duplicate pairs of LcSnRKs. B Collinear gene pairs between the SnRK family of Liriodendron chinense and Arabidopsis thaliana. C Collinear gene pairs between the SnRK family of Liriodendron chinense and rice

Full size image

To explore the homology of the SnRK gene family in L. chinense with that in other species, the homology-collinearity analysis of the SnRK gene in L. chinense, A. thaliana, and rice was performed in this study (Fig. 5). The result showed that 13 LcSnRK genes and AtSnRK genes were in a collinear relationship (Fig. 5B), and 18 LcSnRK genes were collinear with Oryza sativa SnRK (OsSnRK) genes (Fig. 5C). Therefore, it has been suggested that these LcSnRK genes might be involved in the evolution of the LcSnRK gene family. To test the effect of evolutionary constraints, Ka, Ks, and Ka/Ks of paralytic homologous and orthologous pairs on the SnRK gene family were calculated. The Ka/Ks range for the 10 segment-duplicated gene pairs was 0.055 to 0.295 (Additional file 6: Table S3), indicating that all duplicated gene pairs for LcSnRK were purified by selection. The Ks of the 13 homologous gene pairs in L. chinense and A. thaliana were all “NaN”, indicating that the sequences of the gene pairs in L. chinense and A. thaliana had a high score of divergences (Additional file 7: Table S4). The Ka/Ks of the homologous gene pairs in most L. chinense and rice were also much smaller than 1 (Additional file 8: Table S5), suggesting that the LcSnRK gene family may have arisen during evolution by purifying selection.

Protein interaction of SnRKs

Exploring the regulatory network of a gene or a gene family is essential to restore the balance between resistance and growth. Therefore, the interaction network of the LcSnRK protein was analyzed based on its homology with A. thaliana (Fig. 6, Additional file 9: Table S6). In the protein-protein interaction network, it was found that KIN10, SnRK2.3, SnRK2.4, SnRK2.5, OST1, CIPK3, CIPK8, SOS2, CIPK12, SIP3, and CIPK23 existed at the center of the interaction network and served as an important hub, which might play a central role in life activities. In the SnRK1 subfamily, KIN10 can interact with the transcription factor FUSCA3 (FUS3) and some disease-causing related genes PRL. There was also an interaction between three members of this SnRK1 subfamily.

Fig. 6
figure 6

Protein interaction analysis of SnRKs and other proteins. The yellow circles represent the hub gene in the protein-protein interaction network

Full size image

In the SnRK2 subfamily, members of SnRK2 can interact with ABI1; SnRK 2.3/SnRK2.4/SnRK2.5/SnRK2.6 (OST1) can interact with ABI2; In addition, SnRK2.3 can interact with ABI5, suggesting that the ABI family may be closely related to the SnRK2 subfamily. Both SnRK2.4 and SnRK2.5 can interact with two members of the BRCA2 family.

Within the SnRK3 subfamily, a common SOS signaling pathway and a CIPK-CBL complex pathway like the CBL3 (calcineurin B-like protein 3) have been associated with CIPK3, CIPK8, CIPK23, CIPK12, and SIP3. CIPK23 and SIP3 can also activate AKT1 on the potassium channel. All three subfamilies of SnRK can interact with the same gene family (e.g., the PP2C protein phosphatase family). There are also interactions between the three subfamilies of SnRK. For example, ABI1 can simultaneously bind to and interact with KIN10 and OST1, affecting the expression of downstream genes (Fig. 6, Additional file 9: Table S6).

Three-dimensional structures of SnRK proteins

Kinases are widely involved in plant signal transduction in response to various types of stress, including the SnRK gene family. Based on previous studies, some key members of the SnRK family, such as KIN10, OST1, and SOS2, play important roles in the stress response. LcSnRK1.3, LcSnRK2.3, and LcSnRK3.1 showed the highest homology to KIN10, OST1, and SOS2, respectively, and were selected to analyze their three-dimensional structures (Additional file 10: Table S7). From the three-dimensional structure of LcSnRK1.3, it contained a kinase domain and a UBA domain (ubiquitin-related domain), and LcSnRK1.3 also contained the KA1 domain at the C-terminus (Fig. 7A; Additional file 11: Fig. S4).

Fig. 7
figure 7

Three-dimensional structure model of LcSnRK1.3 (A), LcSnRK2.3 (B), LcSnRK3.1 (C)

Full size image

Further modeling and comparing the spatial structure of the LcSnRK1.3 catalytic domain confirmed the significant similarity in the three-dimensional structure between LcSnRK1.3 and KIN10. SnRK2.6/OST1 (Open Stomata 1) was crucial for ABA-induced stomatal closure in response to drought. LcSnRK2.3 contains a conservative kinase domain and a C-terminal regulatory region containing two conservative motifs that form the SnRK2 box. The SnRK2 box forms a single α-helix and runs parallel to the αc-helix (Fig. 7B; Additional file 12: Fig. S5). In addition, like AtOST1, LcSnRK2.3 contains the auto-phosphorylated residues S175 and T176. The highest homology (74%) was found between LcSnRK3.1 and AtSOS2 (Fig. 7C; Additional file 13: Fig. S6). Typical catalytic domains of CIPKs were found in LcSnRK3.1, including an N-terminal kinase catalytic domain, a self-inhibitory motif characteristic of NAF, and a protein kinase 2C-binding domain of PPI. The three-dimensional structure of LcSnRK3.1, which activated the ring of LcSnRK3.1 from its active site, was remarkably similar to AtSOS2.

Expressions of LcSnRKs in response to low-temperature stress

To understand the responses of LcSnRK family individuals to low-temperature stress, transcriptome information from L. chinense elevating under low-temperature stress was selected to analyze the expression design of the LcSnRK quality under low-temperature response (Fig. 8). The low-temperature stress treatment cycle could be roughly divided into continuous up and down-regulation. Expression of 29 LcSnRK genes was detected in the L. chinense cryo transcriptome data, except for the lack of expression of LcSnRK3.2. Four genes of the LcSnRK2 subfamily (LcSnRK2.1/2.2/2.4/2.5) and nine genes of the LcSnRK3 subfamily (LcSnRK3.1/3.6/3.8/3.9/3.11/3.14/3.16/3.17/3.19) were continuously up-regulated. The expression of eight genes (LcSnRK2.1/2.2/2.4/2.5/3.8/3.9/3.11/3.16) increased after 1 day of low temperature stress. The expression of five genes (LcSnRK3.1/3.6/3.14/3.17/3.19) increased after 3 days of low-temperature stress. One gene in the LcSnRK1 subfamily (LcSnRK1.1) and five genes in the LcSnRK3 subfamily (LcSnRK3.3/3.4/3.7/3.18/3.20) were continuously down-regulated.

Fig. 8
figure 8

RNA-seq expression pattern of LcSnRK family genes under low-temperature stress

Full size image

Among them, the expression of four genes decreased after 6 hours of low-temperature stress (LcSnRK1.1/3.7/3.18/3.20), and the expression of two genes decreased after 1 day of low-temperature stress (LcSnRK3.3/3.4). Six genes (LcSnRK1.3/2.3/2.6/3.10/3.12/3.15) were briefly up-and down-regulated, and two genes (LcSnRK1.3/2.3) indicated the highest expression level after 6 hours of low-temperature treatment, followed by the weakness in the expression level.

Four genes (LcSnRK2.6/3.10/3.12/3.15) showed the highest expression level 1 day after low-temperature treatment, while their expression level decreased 3 days later. LcSnRK1.2 expression was stable within 1 day and declined abruptly after 3 days. LcSnRK3.5 expression decreased during the first 6 hours of low-temperature treatment, increased after 6 hours, and decreased to a minimum after 3 days.

To further affirm the expression design of the LcSnRK gene within the over transcriptome investigation, five genes of the LcSnRK2 subfamily (LcSnRK2.1/2.3/2.4/2.5/2.6) and nine genes of the LcSnRK3 subfamily (LcSnRK3.1/3.8/3.9/3.11/3.14/3.16/3.17/3.19/3.21) were chosen for qPCR confirmation. qPCR and RNA-seq were found to have similar expression patterns (Fig. 9). The transcriptome expression of these 14 LcSnRK genes and the expression trend of qPCR were up-regulated, and the expression trend of eight genes (LcSnRK2.1/2.4/2.5/3.8/3.9/3.11/3.14/3.16) in the transcriptome was continuously up-regulated, with a wavelike increase in qPCR. Five genes (LcSnRK2.6/3.1/3.17/3.19/3.21) indicated wavy up-regulation in both transcriptome and qPCR. One gene (LcSnRK2.3) showed a wavelike up-regulation in the transcriptome, and expression in qPCR continued to increase.

Fig. 9
figure 9

Expression patterns of qPCR of LcSnRK family genes under low-temperature stress. Y-axis represents relative expression, and X-axis represents different time points after stress treatment for expression analysis; The mean standard error measurement (SEM) values of three replicates (n = 3) are shown. Each time point was compared with the control group, and the significance was calculated by one-way ANOVA: * means 0.0001 < p < 0.0005, and ** means p < 0.0001

Full size image

Discussion

The SnRK family plays a vital part in plant response reaction signaling pathways and is a keeper in all eukaryotes. SnRK1 is involved in cell energy sensing, while SnRK2 and SnRK3 play fundamental roles in signaling pathways and regulation of gene expression [43, 44]. In later years, different capacities of SnRK family qualities in plants were slowly found and presented in plants [18, 45,46,47], suggesting that the SnRK gene has greater importance in plant life activities. In this research, a total of 30 members of the LcSnRK family were identified from the L. chinense genome. All LcSnRK members contain kinase domains classified according to their different domains and functions as members of the LcSnRK1, LcSnRK2, and LcSnRK3 subfamilies. The six members were classified into the LcSnRK2 subfamily, and LcSnRK2 could be further classified into three classes according to protein sequence and function. This corresponded to the classification of the SnRK2 subfamily in A. thaliana [11, 13, 48]. While the first group of SnRK2s (AtSnRK2.1/4/5/9/10) revealed no effects by ABA, the second group of SnRK2s (AtSnRK2.7/8) revealed fewer effects by ABA, and the third group of SnRK2s (AtSnRK2.2/3/6) revealed highly activated by ABA. Complete activation of OST1 (the highly homologous kinase of LcSnRK2.3) requires a closed conformation of the αC-helix and phosphorylation of the activation loop to allow complete alignment of the catalytic residues in the active conformation. A highly acidic ABA box, an unknown mechanism required for kinase activity, is important for mediating the interaction of SnRK2 with protein phosphatase type 2C (PP2Cs) [22, 49]. S175 and T176 in OST1 face the catalytic site and thus provide the basis for efficient autophosphorylation of OST1, leading to its full activation [50]. LcSnRK3 shares the highest homology with SOS2 among its 21 family members. Recent studies have shown that CIPK24 (SOS2) has basal activity, unlike other members of the CIPK family. At the substrate, the active loop of SOS2 protrudes from the active site, allowing for catalysis. These and other data suggest that securing CIPKs kinase activity requires simultaneous release of the activation loop from the active site and the NAF motif from the nucleotide-binding site [51]. This structure suggests that LcSnRK3.1 is not a self-inhibitory authoritative versicle for CIPKs and represents a compositional highlight of the environment, suggesting that plant homologs may be involved in controlling cytoskeletal structure and function.

The SnRK proteins from rice, A. thaliana, and L. chinense were developed on the same phylogenetic tree using the neighbor-joining strategy to analyze their origin and characteristics. The LcSnRKs were divided into three subgroups and clustered with the corresponding subgroups of rice and A. thaliana during phylogeny. Therefore, three SnRK subgroups must be established before the diversity of dicotyledonous and monocotyledonous plants. Conservative structural motif analysis provided information on the conservation of LcSnRK function during evolution. We found five conservative motifs related to the functional domain in the plant SnRK protein. Motif 2 and 4 contained Ser/Thr active site and ATP-binding region, respectively. Motif 12, motif 14, and motif 8 contain specific conservative domains of SnRK1 (KA1), SNRK23 (glutamine − 303 to proline − 318), and SnRK3 (NAF), respectively. Different patterns of exon-intron structures also play an essential role in the evolution and function of different gene families [52]. SnRK3 subfamily differs in gene number and can divide SnRK3 subfamily into two branches according to the number of introns [53, 54].

Similarly, the LcSnRK3 subfamily can be divided into two branches: intron-rich and intron-poor. In rice and A. thaliana, the SnRK3 subfamily was subdivided according to the number of introns, suggesting that an increase or decrease in the number of introns might promote the structural evolution of the SnRK gene family prior to eudicots-monocots differentiation [54]. Colina et al. [44] found that the SnRK family originates from green algae, and almost all members respond to osmotic stress. The intron-poor group first appeared in the seed plants. If seed plants were subjected to huge natural weights amid advancement, the intron-rich population would lose introns and become an intron-less population [44]. Similar exon-intron patterns and arrangements of conservative motifs indicate a close evolutionary relationship within the same subfamily. In addition, Jeffares et al. [55] found that the density of introns of genes that can be rapidly expressed in stress responses is significantly lower. Liu et al. [56] speculated that intron loss might be an evolution of rapid stress adaptation in the early evolution of land plants. They also suggested that the absence of introns may have facilitated more rapid developmental adaptation in terrestrial organisms. Therefore, it is reasonable to speculate that genes in the intron deletion group in the SnRK3 subfamily become more highly expressed under stress.

Genomic duplication occurs throughout plant advancement and often leads to the extension of gene families [57]. The evolution of angiosperms frequently exhibits two major types of gene duplication patterns known as tandem and segment gene duplication [58] and plays a significant role in gene family expansion [59]. This study found 14 homologous gene pairs within the LcSnRK family, counting 10 sets of segment-duplicate genes and 4 sets of gene clusters. In addition, we identified 13 pairs of homologous gene pairs between L. chinense and A. thaliana and 18 pairs between L. chinense and rice. The SnRK2 and SnRK3 subfamilies are plant-specific and arise through duplication of the SnRK1 family [43, 44]. The expansion of the SnRK family is likely because large plants are sessile organisms subject to greater biotic and abiotic pressures than animals [44]. The Ka/Ks ratio of the full-length encoded protein sequences of 14 pairs from collateral homologous gene pairs was much lower than 1, indicating that most genes were effectively purified and selected.

Tissue- and time-specific expression patterns of genes in growing plants often reflect differences in the biological function of gene family members and interactions between related signaling pathways [60, 61]. At the transcriptional level, a total of 21 genes in the LcSnRK family continuously increased or decreased under low-temperature stress. The expression of one member of the LcSnRK1 subfamily decreased with increasing low-temperature stress, while that of four members of the LcSnRK2 subfamily increased with increasing low-temperature stress. The expression of 14 genes of the LcSnRK3 subfamily increased or decreased with increasing low-temperature stress. Regarding evolutionary position, LcSnRK2.5 and LcSnRK2.6 were the closest to OsSAPK8 in rice (Fig. 1B). The rice ossapk8 mutant exhibited slow growth and yellowing of leaves under low temperature treatment [62]. Moreover, from the expression pattern of L. chinense leaves under low temperature treatment, the expression of LcSnRK2.5 reached its highest at 6 hours after low-temperature treatment. It then declined but rose 3 days later. The expression of LcSnRK2.6 reached its peak at 3 days of low temperature treatment. In addition, when Agropyron cristatum AcSnRK2.11 was transferred to tobacco, the transgenic plants indicated stronger cold resistance [63]. LcSnRK3.5/3.6/3.7/3.19 is closer to AtCIPK7 in evolutionary terms (Fig. 1B). In A. thaliana, CIPK7 can interact with CBL1 in vivo and in vitro to play a role in the low-temperature response [64]. Under low-temperature treatment, the expression of LcSnRK3.19 reached its peak 6 hours after low-temperature treatment and then declined but increased after 3 days. In addition, AcCIPK5, a cognate gene of AtCIPK12, positively regulated the cold tolerance of A. thaliana in Ananas comosus (L.) [65]. Consequently, we can conclude that individuals of the SnRK2 and SnRK3 subfamilies are more likely to be interested in the low-temperature response reaction in L. chinense.

Similarly, in the promoter sequence of the LcSnRK gene, many cis-acting elements associated with low temperature and other abiotic stresses, such as LTR and TC-rich repeats, were found. These results indicated that the LcSnRK gene might respond to abiotic stress, particularly low-temperature stress. In addition, LcSnRK1.3, LcSnRK2.3, and LcSnRK3.1 shared high homology with KIN10, OST1, and SOS2, respectively, in A. thaliana. The studies on KIN10, OST1, and SOS2 in A. thaliana were in-depth [1, 66, 67]. KIN10 is the central integron of the transcriptional network involved in stress and energy signal transduction in plants [1, 68, 69], which can be associated with other family proteins in reaction to abiotic response in plants. OST1 may be involved in the signaling pathway in plants in response to abiotic stress through phosphorylation [70, 71]. The CBL-CIPK (SnRK3) complex is involved in the signal transduction of various stresses. SOS2 physically interacts with the calcium sensor SOS3 [72] and is activated in a calcium-dependent manner [73]. Therefore, the expression of these three genes under abiotic stress indicates certain regularity based on the transcriptional level expression results. For case, LcSnRK1.1 expression was persistently up-regulated under low-temperature stress, and LcSnRK2.3 expression appeared to be a short-term expanding drift under low-temperature stress. LcSnRK3.1 expression was ceaselessly up-regulated under low-temperature response. These three genes may be essential in studying the L. chinense response to low-temperature stress.

Conclusions

The genes of the SnRK family play essential roles in signaling pathways such as plant response to biotic and abiotic stresses. In this study, 30 members of the SnRK gene family were identified in L. chinense and divided into three typical subfamilies with the same features and obvious differences in gene structure and motif composition. In response to L. chinense to low-temperature stress, the 30 members of the SnRK gene family had four expression patterns, and the expression trend of 14 genes was continuously increased while that of 6 genes was decreased. These results will give imperative data for examining the structural characteristics and potential natural capacities of the LcSnRK gene in L. chinense.

Materials and methods

Documentation and physicochemical properties analysis of LcSnRKs

The nucleic acid and protein sequences of L. chinense were obtained from the L. chinense protein database (https://hardwoodgenomics.org/) [74]. Protein sequences from the SnRK family of A. thaliana and rice were downloaded from the Phytozome database (https://phytozome-next.jgi.doe.gov/) [75], and the rice annotation project (RAP) (https://rapdb.dna.affrc.go.jp/) [76], respectively. Local BLASTP searches were completed using the SnRK protein sequences from A. thaliana and rice. The Hidden Markov Model (HMM) and the BLASTP program were used for the preliminary identification of LcSnRK family proteins. LcSnRK candidate proteins were further validated by the NCBI conservative domain database, the SMART database, and the Pfam database (http://pfam.xfam.org/) for domain search [77]. Based on the information in the above three databases, the LcSnRK gene with the traditional domain was manually screened. The online software Protparam in the Expasy database (https://web.expasy.org/protparam/) was used to identify sequences of SnRK of L. chinense, the physicochemical properties (including molecular weight, isoelectric point, and hydrophilicity) [78]. Signal peptides of the LcSnRK protein were predicted using SignalP (https://services.healthtech.dtu.dk/service.php?SignalP). Subcellular localization of the LcSnRK protein was predicted by Plant-mPLoc (http://www.csbio.sjtu.edu.cn/bioinf/plant-multi/) [79].

Phylogenetic analysis of LcSnRKs

Phylogenetic analysis was performed using the SnRK members from L. chinense, Rice, and A. thaliana. The multiple sequences were aligned using ClustalX. The phylogenetic tree was assembled using the NJ method in the MEGA7.0 software [80]. Evolutionary distances were obtained using the p-distance method, which was used to estimate the number of amino acids in each locus. One thousand bootstrap sampling iterations guaranteed the reliability of each phylogenetic tree. iTOL was used for further beautification.

Chromosome location and gene duplication analysis of LcSnRKs

According to the physical location information in the L. chinense genome database, the identified LcSnRK gene was chromosomally localized using the biological software TBtools [81]. To analyze the duplication events of the LcSnRK gene, all L. chinense genomic sequences were aligned with BLASTP. The duplication modes of SnRK were divided into segment duplication and tandem duplication using MCScanX [82]. Finally, the collinear analysis diagram was constructed using the Circos software [83]. Nonsynonymous (Ka) and synonymous (Ks) substitutions between pairs of interest were calculated using the KaKs_Calculator [84].

Gene structure, conservative motif, and cis-regulation elements of LcSnRKs

The intron-exon structures of the LcSnRKs were mapped onto the diagrams using the annotation files in the L. chinense genome database by TBtools software. The conserved motifs of the SnRK protein in L. chinense were analyzed online by MEME (https://meme-suite.org/meme/doc/meme.html) using the predicted full-length protein sequences of the LcSnRKs. Extracting an upstream sequence (2000 bp) of an initiation codon of each LcSnRK gene from L. chinense genomic sequence. PlantCare (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) [85] was then used to predict the distribution of cis-acting elements in the promoter region of LcSnRKs.

Protein-protein interaction network prediction of SnRKs

Based on the high homology between LcSnRKs and AtSnRKs proteins, a String database (https://cn.string-db.org/) was used to generate a functional protein interaction network. The protein interaction network of the SnRK family was plotted using Cytoscape 3.8.2 [86].

Three-dimensional structure modeling and verification of LcSnRK proteins

The full-length atomic structure of the LcSnRK protein was assembled by the Robetta program (https://robetta.bakerlab.org/) to construct the structure of the protein. The structure of the candidate protein was further explored since the reliability of its protein structure was determined using the online website SAVESv6.0 (https://saves.mbi.ucla.edu/) including ERRAT, PROVE, Ramachandran. Then the 3D modeling was performed using VMD software.

Expression analysis of LcSnRKs based on transcriptome and qRT-PCR

The expression of LcSnRK in response to cold stress was analyzed using the methods of Guan et al. [87] and Li et al. [88] and momentarily attuned. Two-month-old and identically growing Liriodendron hybrid seedlings regenerated from somatic embryos were transferred to an incubator (25 °C, 16 h light, and 8 h dark) for culture for 1 week and then transferred to a 4 °C incubator for low-temperature stress treatment. Leaves were detached at 0 h, 6 h, 24 h, and 3 days after cold stress treatment for transcriptome sequencing and qRT-PCR analysis. The RNA was extracted using FastPure® Plant Total RNA Isolation Kit (Polysaccharides&Polyphenolics-rich) (Vazyme, Nanjing, China). RNA purity was checked using the NanoPhotometer® spectrophotometer (IMPLEN, CA, USA). RNA integrity was assessed using the RNA Nano 6000 Assay Kit of the Bioanalyzer 2100 system (Agilent Technologies, CA, USA). The library preparations were sequenced on an Illumina Novaseq 6000 platform, and 150 bp paired-end reads were generated [89]. Three replicates were set for each independent experiment. The housekeeping L. chinense 18S gene was used as an internal control. All qRT-PCR primers were designed by Primer5.0 (Additional file 14: Table S8). All data generated from real-time PCR amplification was analyzed using a 2−△△CT method.

Availability of data and materials

The datasets generated and/or analysed during the current study are available in the [NCBI website] repository, [https://www.ncbi.nlm.nih.gov/assembly/GCA_003013855.2]. The qRT-PCR data supporting the gene relative expression results of this study can be found in Additional file 14. The transcriptome data used in this study has been archived and can also be obtained on the NCBI website. The cold stress accession numbers were PRJNA679089 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA679089/).

Abbreviations

SnRK:

The sucrose non-fermenting 1 (SNF1)-related protein kinases

KA1:

Kinase associated-1 domain

UBA:

Ubiquitin-associated domain

NAF:

National Arbitration Forum Domain

KIN10:

SNF1 kinase homolog 10 protein kinase

KIN11:

SNF1 kinase homolog 11 protein kinase

OST1:

OPEN STOMATA 1 protein kinase

CIPK:

Calcineurin B like protein-interacting protein kinase

SOS2:

SALT OVERLY SENSITIVE 2 protein kinase

bZIP63:

BASIC LEUCINE ZIPPER 63 Transcription factor

ABA:

Abscisic acid

qRT-PCR:

Quantitative real-time polymerase chain reaction

References

  1. Baena-González E, Rolland F, Thevelein JM, Sheen J. A central integrator of transcription networks in plant stress and energy signalling. Nature. 2007;448(7156):938–42. https://doi.org/10.1038/nature06069.

    Article  CAS  PubMed  Google Scholar 

  2. Lin Z, Li Y, Zhang Z, Liu X, Hsu CC, Du Y, et al. A RAF-SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat Commun. 2020;11(1):613. https://doi.org/10.1038/s41467-020-14477-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Takahashi Y, Zhang J, Hsu PK, Ceciliato PHO, Zhang L, Dubeaux G, et al. MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat Commun. 2020;11:12.

    Article  CAS  Google Scholar 

  4. Lin Z, Li Y, Wang Y, Liu X, Ma L, Zhang Z, et al. Initiation and amplification of SnRK2 activation in abscisic acid signaling. Nat Commun. 2021;12(1):2456. https://doi.org/10.1038/s41467-021-22812-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 2003;132:666–80.

    Article  CAS  Google Scholar 

  6. Hofmann K, Bucher P. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci. 1996;21:172–3.

    Article  CAS  Google Scholar 

  7. Bhalerao RP, Salchert K, Bakó L, Okrész L, Szabados L, Muranaka T, et al. Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc Natl Acad Sci U S A. 1999;96(9):5322–7. https://doi.org/10.1073/pnas.96.9.5322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Farra's R, Ferrando A, Ja'sik J, Kleinow T, Okre'sz L, Tiburcio A, et al. SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J. 2001;20:2742–56.

    Article  CAS  Google Scholar 

  9. Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A, Martinho C, et al. ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell. 2013;25:3871–84.

    Article  CAS  Google Scholar 

  10. Jamsheer KM, Jindal S, Laxmi A. Evolution of TOR-SnRK dynamics in green plants and its integration with phytohormone signaling networks. J Exp Bot. 2019;70(8):2239–59. https://doi.org/10.1093/jxb/erz107.

    Article  CAS  Google Scholar 

  11. Kulik A, Wawer I, Krzywinska E, et al. SnRK2 protein kinases—key regulators of plant response to abiotic stresses. OMICS. 2011;15(12):859–72.

    Article  CAS  Google Scholar 

  12. Kobayashia Y, Yamamotoa S, Minamia H, et al. Differential activation of the rice sucrose nonfermenting1-related protein kinase 2 family by hyperosmotic stress and abscisic acid. Plant Cell. 2004;16:1163–77.

    Article  Google Scholar 

  13. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem. 2006;281:5310–8.

    Article  CAS  Google Scholar 

  14. Albrecht V, Ritz O, Linder S, Harter K, Kudla J. The NAF domain defines a novel protein-protein interaction module conserved in Ca2+−regulated kinases. EMBO. 2001;J20(5):1051–63.

    Article  Google Scholar 

  15. Ohta M, Guo Y, Halfter U, Zhu JK. A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci U S A. 2003;100(20):11771–6.

    Article  CAS  Google Scholar 

  16. Halford NG, Hardie DG. SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol Biol. 1998;37(5):735–48.

    Article  CAS  Google Scholar 

  17. Bai Y, Meng Y, Huang D, et al. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics. 2011;98(2):128–36.

    Article  CAS  Google Scholar 

  18. Henninger M, Pedrotti L, Krischke M, Draken J, Wildenhain T, Fekete A, et al. The evolutionarily conserved kinase SnRK1 orchestrates resource mobilization during Arabidopsis seedling establishment. Plant Cell. 2022;34(1):616–32. https://doi.org/10.1093/plcell/koab270.

    Article  PubMed  Google Scholar 

  19. Muralidhara P, Weiste C, Collani S, Krischke M, Kreisz P, Draken J, et al. Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-bZIP63-ARF19 signaling. Proc Natl Acad Sci U S A. 2021;118(37):e2106961118. https://doi.org/10.1073/pnas.2106961118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhang H, Zhao Y, Zhu JK. Thriving under stress: how plants balance growth and the stress response. Dev Cell. 2020;55(5):529–43. https://doi.org/10.1016/j.devcel.2020.10.012.

    Article  CAS  PubMed  Google Scholar 

  21. Han C, Liu Y, Shi W, Qiao Y, Wang L, Tian Y, et al. KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor. Nat Commun. 2020;11(1):4214. https://doi.org/10.1038/s41467-020-18048-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Boudsocq M, Barbier-Brygoo H, Laurière C. Identification of nine sucrose non-fermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J Biol Chem. 2004;279(40):41758–66. https://doi.org/10.1074/jbc.M405259200.

    Article  CAS  PubMed  Google Scholar 

  23. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, et al. In vitro reconstitution of an abscisic acid signalling pathway. Nature. 2009;462:660–4.

    Article  CAS  Google Scholar 

  24. Soma F, Takahashi F, Suzuki T, Shinozaki K, Yamaguchi-Shinozaki K. Plant Raf-like kinases regulate the mRNA population upstream of ABA-unresponsive SnRK2 kinases under drought stress. Nat Commun. 2020;11(1):1373. https://doi.org/10.1038/s41467-020-15239-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen Q, Hu T, Li X, Song CP, Zhu JK, Chen L, et al. Phosphorylation of SWEET sucrose transporters regulates plant root: shoot ratio under drought. Nat Plants. 2021. https://doi.org/10.1038/s41477-021-01040-7.

  26. Kim KN, Lee JS, Han H, Choi SA, Go SJ, Yoon IS. Isolation and characterization of a novel rice Ca2+−regulated protein kinase gene involved in responses to diverse signals including cold, light, cytokinins, sugars, and salts. Plant Mol Biol. 2003;52:1191–202.

    Article  CAS  Google Scholar 

  27. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A. 2000. https://doi.org/10.1073/pnas.97.7.3730.

  28. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell. 2002;3:233–44.

    Article  CAS  Google Scholar 

  29. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, et al. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 inArabidopsis. Cell. 2006;125:1347–60. https://doi.org/10.1016/j.cell.2006.06.011.

    Article  CAS  PubMed  Google Scholar 

  30. Li LG, Kim BG, Cheong YH, Pandey GK, Luan S. A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci U S A. 2006;103:12625–30.

    Article  CAS  Google Scholar 

  31. Ragel P, et al. The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol. 2015;169:2863–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Scherzer S, et al. Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps. Proc Natl Acad Sci U S A. 2015;112:7309–14.

    Article  CAS  Google Scholar 

  33. Tang RJ, Zhao FG, Yang Y, Wang C, Li K, Kleist TJ, et al. A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments. Nat Plants. 2020;6(4):384–93. https://doi.org/10.1038/s41477-020-0621-7.

    Article  CAS  PubMed  Google Scholar 

  34. Ma QJ, Sun MH, Kang H, Lu J, You CX, Hao YJ. A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser254 for phosphorylation to enhance salt tolerance. Plant Cell Environ. 2019a;42(3):918–30. https://doi.org/10.1111/pce.13349.

    Article  CAS  PubMed  Google Scholar 

  35. Ma QJ, Sun MH, Lu J, Kang H, You CX, Hao YJ. An apple sucrose transporter MdSUT2.2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought. Plant Biotechnol J. 2019b;17(3):625–37. https://doi.org/10.1111/pbi.13003.

    Article  CAS  PubMed  Google Scholar 

  36. Yan J, Niu F, Liu WZ, Zhang H, Wang B, Lan W, et al. Arabidopsis CIPK14 positively regulates glucose response. Biochem Biophys Res Commun. 2014;450(4):1679–83. https://doi.org/10.1016/j.bbrc.2014.07.064.

    Article  CAS  PubMed  Google Scholar 

  37. Barajas-Lopez JD, Moreno JR, Gamez-Arjona FM, Pardo JM, Punkkinen M, Zhu JK, et al. Upstream kinases of plant SnRKs are involved in salt stress tolerance. Plant J. 2018;93(1):107–18. https://doi.org/10.1111/tpj.13761.

    Article  CAS  PubMed  Google Scholar 

  38. Zhao W, Cheng YH, Zhang C, Shen XJ, You QB, Guo W, et al. Genome-wide identification and characterization of the GmSnRK2 family in soybean. Int J Mol Sci. 2017;18(9):1834. https://doi.org/10.3390/ijms18091834.

    Article  CAS  PubMed Central  Google Scholar 

  39. Zhang YH, Wan SQ, Wang WD, Chen JF, Huang LL, Duan MS, et al. Genome-wide identification and characterization of the CsSnRK2 family in Camellia sinensis. Plant Physiol Biochem. 2018;132:287–96. https://doi.org/10.1016/j.plaphy.2018.09.021.

    Article  CAS  PubMed  Google Scholar 

  40. Zhu W, Wu D, Jiang L, Ye L. Genome-wide identification and characterization of SnRK family genes in Brassica napus. BMC Plant Biol. 2020;20(1):287. https://doi.org/10.1186/s12870-020-02484-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cao Y, Feng J, Hwarari D, Ahmad B, Wu H, Chen J, et al. Alterations in population distribution of Liriodendron chinense (Hemsl.) Sarg. And Liriodendron tulipifera Linn. Caused by Climate Change. Forests. 2022;13(3):488. https://doi.org/10.3390/f13030488.

    Article  Google Scholar 

  42. Collins RL, Brand H, Karczewski KJ, Zhao X, Alföldi J, Francioli LC, et al. A structural variation reference for medical and population genetics. Nature. 2020;581(7809):444–51. https://doi.org/10.1038/s41586-020-2287-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Halford NG, Hey SJ. Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J. 2009;419(2):247–59. https://doi.org/10.1042/BJ20082408.

    Article  CAS  PubMed  Google Scholar 

  44. Colina F, Amaral J, Carbó M, et al. Genome-wide identification and characterization of CKIN/SnRK gene family in Chlamydomonas reinhardtii. Sci Rep. 2019;9:350. https://doi.org/10.1038/s41598-018-35625-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cui F, Brosché M, Lehtonen MT, Amiryousefi A, Xu E, Punkkinen M, et al. Dissecting abscisic acid signaling pathways involved in cuticle formation. Mol Plant. 2016;9(6):926–38. https://doi.org/10.1016/j.molp.2016.04.001.

    Article  CAS  PubMed  Google Scholar 

  46. Wang W, Lu Y, Li J, Zhang X, Hu F, Zhao Y, et al. SnRK1 stimulates the histone H3K27me3 demethylase JMJ705 to regulate a transcriptional switch to control energy homeostasis. Plant Cell. 2021;33(12):3721–42. https://doi.org/10.1093/plcell/koab224.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Kamiyama Y, Hirotani M, Ishikawa S, Minegishi F, Katagiri S, Rogan CJ, et al. Arabidopsis group C Raf-like protein kinases negatively regulate abscisic acid signaling and are direct substrates of SnRK2. Proc Natl Acad Sci U S A. 2021;118(30):e2100073118. https://doi.org/10.1073/pnas.2100073118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Belin C, de Franco PO, Bourbousse C, Chaignepain S, Schmitter JM, Vavasseur A, et al. Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 2006;141(4):1316–27. https://doi.org/10.1104/pp.106.079327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Boudsocq M, Droillard MJ, Barbier-Brygoo H, Laurière C. Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol Biol. 2007;63:491–503.

    Article  CAS  Google Scholar 

  50. Ng LM, Soon FF, Zhou XE, West GM, Kovach A, Suino-Powell KM, et al. Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci U S A. 2011;108(52):21259–64. https://doi.org/10.1073/pnas.1118651109.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Chaves-Sanjuán A, Sánchez-Barrena MJ, González-Rubio JM, Albert A. Preliminary crystallographic analysis of the ankyrin-repeat domain of Arabidopsis thaliana AKT1: identification of the domain boundaries for protein crystallization. Acta Crystallogr F Struct Biol Commun. 2014;70(Pt 4):509–12. https://doi.org/10.1107/S2053230X14005093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Jo BS, Choi SS. Introns: the functional benefits of introns in genomes. Genomics Inform. 2015;13(4):112–8. https://doi.org/10.5808/GI.2015.13.4.112.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX, et al. Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 2015;112:3134–9. https://doi.org/10.1073/pnas.1420944112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Zhu JK. Abiotic stress signaling and responses in plants. Cell. 2016;167(2):313–24. https://doi.org/10.1016/j.cell.2016.08.029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Jeffares DC, Penkett CJ, Bähler J. Rapidly regulated genes are intron poor. Trends Genet. 2008;24:375–8.

    Article  CAS  Google Scholar 

  56. Liu D, Zhao H, Xiao Y, Zhang G, Cao S, Yin W, et al. A cryptic inhibitor of cytokinin phosphorelay controls rice grain size. Mol Plant. 2021. https://doi.org/10.1016/j.molp.2021.09.010.

  57. Mehan MR, Freimer NB, Ophoff RA. A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture. Hum Genomics. 2004;1(5):335–44.

    Article  CAS  Google Scholar 

  58. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290:1151–5. https://doi.org/10.1126/science.290.5494.1151.

    Article  CAS  PubMed  Google Scholar 

  59. Cannon S, Mitra A, Baumgarten A, Young N, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4(1):1–21.

    Article  Google Scholar 

  60. Hu CH, Wei XY, Yuan B, Yao LB, Ma TT, Zhang PP, et al. Genome-wide identification and functional analysis of NADPH oxidase family genes in wheat during development and environmental stress responses. Front Plant Sci. 2018;9:906. https://doi.org/10.3389/fpls.2018.00906.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Zhao Y, Zhou M, Xu K, Li J, Li S, Zhang S, et al. Integrated transcriptomics and metabolomics analyses provide insights into cold stress response in wheat. Crop. 2019;J.7:857–66. https://doi.org/10.1016/j.cj.2019.09.002.

    Article  Google Scholar 

  62. Zhong RL, Wang YX, Gai RN, et al. Rice SnRK protein kinase OsSAPK8 acts as a positive regulator in abiotic stress responses. Plant Sci. 2020;292:110373. https://doi.org/10.1016/j.plantsci.2019.110373.

    Article  CAS  PubMed  Google Scholar 

  63. Xiang DJ, Man LL, Cao S, et al. Heterologous expression of an Agropyron cristatum SnRK2 protein kinase gene (AcSnRK2.11) increases freezing tolerance in transgenic yeast and tobacco. 3. Biotech. 2020;10(5):209. https://doi.org/10.1007/s13205-020-02203-7.

    Article  Google Scholar 

  64. Huang C, Ding S, Zhang H, Du H, An L. CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci. 2011;181(1):57–64. https://doi.org/10.1016/j.plantsci.2011.03.011.

    Article  CAS  PubMed  Google Scholar 

  65. Aslam M, Greaves JG, Jakada BH, Fakher B, Wang X, Qin Y. AcCIPK5, a pineapple CBL-interacting protein kinase, confers salt, osmotic and cold stress tolerance in transgenic Arabidopsis. Plant Sci. 2022;320:111284, ISSN 0168-9452. https://doi.org/10.1016/j.plantsci.2022.111284.

    Article  CAS  PubMed  Google Scholar 

  66. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell. 2002;14:3089–99.

    Article  CAS  Google Scholar 

  67. Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratge-Faillie C, et al. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res. 2011;21:1116–30.

    Article  CAS  Google Scholar 

  68. Baena-González E, Sheen J. Convergent energy and stress signaling. Trends Plant Sci. 2008;13(9):474–82. https://doi.org/10.1016/j.tplants.2008.06.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Smeekens S, Ma J, Hanson J, Rolland F. Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol. 2010;13:274–9.

    Article  CAS  Google Scholar 

  70. Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y, et al. Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol. 2009;16:1230–6.

    Article  CAS  Google Scholar 

  71. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell. 2015;32(3):278–89. https://doi.org/10.1016/j.devcel.2014.12.023.

    Article  CAS  PubMed  Google Scholar 

  72. Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science. 1998;280:1943–5.

    Article  CAS  Google Scholar 

  73. Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci U S A. 2000;97:3735–40.

    Article  CAS  Google Scholar 

  74. Chen J, Hao Z, Guang X, Zhao C, Wang P, Xue L, et al. Liriodendron genome sheds light on angiosperm phylogeny and species-pair differentiation. Nat Plants. 2019;5(1):18–25. https://doi.org/10.1038/s41477-018-0323-6.

    Article  CAS  PubMed  Google Scholar 

  75. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40:D1202–10. https://doi.org/10.1093/nar/gkr1090.

    Article  CAS  PubMed  Google Scholar 

  76. Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, et al. Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol. 2013;54:e6. https://doi.org/10.1093/pcp/pcs183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44(D1):D279–85. https://doi.org/10.1093/nar/gkv1344.

    Article  CAS  PubMed  Google Scholar 

  78. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, et al. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 2012;40(Web Server issue):W597–603. https://doi.org/10.1093/nar/gks400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Chou KC, Shen HB. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One. 2010;5(6):e11335. https://doi.org/10.1371/journal.pone.0011335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.

    Article  CAS  Google Scholar 

  81. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202. https://doi.org/10.1016/j.molp.2020.06.009.

    Article  CAS  PubMed  Google Scholar 

  82. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40:49.

    Article  Google Scholar 

  83. Voorrips RE. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93:77–8.

    CAS  PubMed  Google Scholar 

  84. Wang D, Zhang Y, Zhang Z, Zhu J, Yu J. KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics. 2010;8(1):77–80. https://doi.org/10.1016/S1672-0229(10)60008-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Yves VDP, et al. Plantcare, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30:325–7.

    Article  CAS  Google Scholar 

  86. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504. https://doi.org/10.1101/gr.1239303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Guan YL, Liu SQ, Wu WH, Hong KY, Li RX, Zhu LM, et al. Genome-wide identification and cold stress-induced expression analysis of the CBF gene family in Liriodendron chinense. J For Res. 2021;32. https://doi.org/10.1007/s11676-020-01275-8.

  88. Li R, Ahmad B, Hwarari D, Li D, Lu Y, Gao M, et al. Genomic survey and cold-induced expression patterns of bHLH transcription factors in Liriodendron chinense (Hemsl) Sarg. Forests. 2022;13(4):518. https://doi.org/10.3390/f13040518.

    Article  Google Scholar 

  89. Wu W, Zhu S, Xu L, Zhu L, Wang D, Liu Y, et al. Genome-wide identification of the Liriodendron chinense WRKY gene family and its diverse roles in response to multiple abiotic stress. BMC Plant Biol. 2022;22(1):25. https://doi.org/10.1186/s12870-021-03371-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Not applicable.

Funding

This research was funded by the National Natural Science Foundation of China (No. 31971682), the Research Startup Fund for High-Level and High-Educated Talents of Nanjing Forestry University, and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Authors and Affiliations

  1. College of Biology and the Environment, Nanjing Forestry University, Nanjing, 210037, China

    Rongxue Li, Yasmina Radani, Ali Movahedi & Liming Yang

  2. Muhammad Nawaz Sharif University of Agriculture, Multan, Punjab, 25000, Pakistan

    Baseer Ahmad

Authors
  1. Rongxue Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasmina Radani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baseer Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ali Movahedi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liming Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LY designed the research. RL conducted experiments. RL and RY contributed analytic tools and manuscript writing. LY, AM, and BA manuscript revision and editing. LY source funding. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Ali Movahedi or Liming Yang.

Ethics declarations

Ethics approval and consent to participate

The Liriodendron hybrid seedlings regenerated from somatic embryos were grown and collected in the greenhouse in Nanjing Forestry University (Nanjing, Jiangsu province, China). All samples from the cultivar were adopted for all experiments.

These plant materials do not include any wild species at risk of extinction.

No specific permits are required for sample collection in this study. We comply with the IUCN Policy Statement on Research Involving Species at Risk of Extinction and the Convention on the Trade in Endangered Species of Wild Fauna and Flora.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

Basic protein information of LcSnRK family members.

Additional file 2: Fig. S1. 

Phylogenetic tree of LcSnRKs. The scale of the length of each branch is labeled at the bottom of the graph, and the bootstrap value of each branch is labeled at the node position.

Additional file 3: Table S2.

Details of the SnRK gene family for rice and Arabidopsis.

Additional file 4: Fig. S2.

15 Conservative motifs logo of LcSnRKs.

Additional file 5: Fig. S3.

The detailed distribution of each cis-acting element in the promoter region.

Additional file 6: Table S3.

The segmental and tandem duplication events of LcSnRKs.

Additional file 7: Table S4.

The Ka/Ks ratios between L.chinenese and Arabidopsis thaliana.

Additional file 8: Table S5.

The Ka/Ks ratios between L.chinenese and Oryza sativa.

Additional file 9: Table S6.

Detailed information of interaction network of LcSnRKs with other proteins.

Additional file 10: Table S7.

Alignment of protein sequences of LcSnRK and AtSnRK family members.

Additional file 11: Fig. S4.

Sequence alignment of AKIN10 and LcSnRK1.3 protein. Conservative sites in the activation loop are indicated by a red asterisk, and UBA and KA1 are conservative domains in the SnRK1 subfamily, respectively. Differently colored line segments highlight completely conservative and potential phosphorylated residues.

Additional file 12: Fig. S5.

Sequence alignment of AtOST1 and LcSnRK2.3 protein. Conservative sites in the activation loop are indicated by a red asterisk. Differently colored line segments highlight completely conservative and potential phosphorylated residues.

Additional file 13: Fig. S6.

Sequence alignment of AtSOS2 and LcSnRK3.1 proteins. Differently colored line segments highlight completely conservative and potential phosphorylated residues.

Additional file 14: Table S8.

The primers used in the qRT-PCR

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, R., Radani, Y., Ahmad, B. et al. Identification and characteristics of SnRK genes and cold stress-induced expression profiles in Liriodendron chinense. BMC Genomics 23, 708 (2022). https://doi.org/10.1186/s12864-022-08902-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12864-022-08902-0

Keywords

BMC Genomics

ISSN: 1471-2164

Contact us