Genome-wide identification of the potato GGPS gene family and analysis of its response to abiotic stress

doi:10.21203/rs.3.rs-5028362/v1

Background: Geranylgeranyl pyrophosphate synthase (GGPS) plays a crucial role in terpene biosynthesis, contributing to the synthesis of carotenoids, chlorophylls, and various phytohormones. This study aims to identify and characterize the GGPS gene family in potato (Solanum tuberosum) to understand its role in carotenoid synthesis and response to abiotic stress.

Results: Eleven GGPS genes (StGGPSs) were identified across the potato genome, distributed unevenly on seven chromosomes. These genes were categorized into three subfamilies based on protein structure and phylogenetic analysis. Covariance analyses revealed one pair of replicated genes within the potato genome and several homologous pairs between potato and other species such as Arabidopsis and tomato. RNA-seq data and qPCR data indicated differential expression of StGGPS genes in potato patches of different colors, highlighting their role in response to abiotic stresses.

Conclusion: The study provides new insights into the evolution of the StGGPS gene family in potato, emphasizing its significance in regulating carotenoid synthesis and abiotic stress response. These findings lay the groundwork for future research on the genetic manipulation of GGPS genes to enhance stress tolerance in potatoes.

potato

GGPS gene family

carotenoid synthesis

abiotic stress

expression analysis

Carotenoids are widely distributed terpenoid pigments found in bacteria, fungi, algae and terrestrial plants, playing essential roles in plant photosynthesis and photoprotection[1–6]. Within photosynthetic membranes, carotenoids bind to proteins, forming pigment-protein complexes that function as light-harvesting pigments[7]. Additionally, carotenoids contribute to plant development and stress resistance by acting as sources of retrograde signals[8]. For instance, carotenoids are precursors in the synthesis of abscisic acid through the MEP pathway[9], which helps plants resist abiotic stresses such as drought and salinity[10]. Strigolactones, another class of carotenoid derivatives, regulate grant growth by inhibiting branching, shaping root architecture, and promoting leaf development. They play important roles in regulating aging and secondary growth[11].

Geranylgeranyl pyrophosphate synthase (GGPS) is a key enzyme in the biosynthesis of terpenoids, catalyzing the formation of geranylgeranyl pyrophosphate (GGPP) from farnesyl pyrophosphate (FPP) and isopentenyl pyrophosphate (IPP)[12]. GGPP serves as a precursor for the synthesis of important plant pigments and hormones, including carotenoids, chlorophyll, gibberellin, and abscisic acid[13]. GGPS has been shown to play crucial roles in various plants, such as in chlorophyll synthesis in cotton[14], terpenoid synthesis in tulips[15], and carotenoid biosynthesis in sweet potato, where it may contribute to osmotic stress tolerance[16].

Potato (Solanum tuberosum), the most productive non-cereal food crop, is a vital source of carbohydrates, dietary fiber, vitamins, and antioxidants[17]. Despite its nutritional benefits, potato cultivation is highly vulnerable to t abiotic stresses (e.g., heat stress, drought, salinity) and biotic stresses (e.g., insect infestation)[18]. GGPS, as a key enzyme in beta-carotene, gibberellin, and chlorophyll synthesis, has the potential to enhance potato resistance to these stresses. However, while GGPS gene families have been identified in various plants, their biological functions in potatoes remain unexplored.

To address this gap, this study aims to comprehensively analyze the potato GGPS gene family by examining chromosomal locations, physicochemical properties, gene structure, conserved motifs, and duplication events. We utilized RNA-seq data to identify candidate StGGPS genes that respond to abiotic stresses and further analyzed their expression patterns under different stress conditions. This study seeks to elucidate the roles of the StGGPS gene family in potato resistance, providing new insights into their potential applications in improving potato resilience.

RNA extraction and qRT-PCR analysis

The potato variety, Jinong Shu 8511, bred by the Agricultural University of Hebei, served as the experimental material for this study. The plants, characterized by yellow skin and flesh, were grown for 21 days before being subjected to stress conditions. To simulate drought stress, seedlings were treated with 25 mmol/L PEG6000, and to simulate salt stress, 70 mmol/L of NaCl was used. Samples were collected at 0, 12, and 24 h post-stress, flash-frozen in liquid nitrogen, and stored at − 80 ° C.

Total RNA was extracted using the Promega RNA Extraction kit (LS1040), and RNA integrity and concentration were assessed through agarose gel electrophoresis and a Nanodrop ND-2000 spectrophotometer (Nanodrop Technologies, USA). First-strand cDNA synthesis was performed using the Kangwei Century RT gDNA kit (CW2020M). qRT-PCR was carried out on a CFX96 system (Bio-Rad, USA) using the US EVERBRIGHT (AugeGreen qPCR Master Mix S2008L) kit. The reaction conditions were based on the AugeGreen qRT-PCR Master Mix instructions. Reactions were run in three biological replicates and three technical replicates. StEF-1α was used as the reference gene[19], and relative expression was calculated using the 2^-ΔΔct methods[20].

Identification and Sequence analysis of Potato GGPS Genes

The genome annotation files and nucleotide sequences for Solanum tuberosum were downloaded from the Ensembl Plant database (http://plants.ensembl.org/index.html). The GGPS structural domain (PF00348) was identified using HMMER 3.1 (http://hmmer.org/download.html) within the potato genome protein sequences. Sequences lacking the GGPS structural domain were excluded, and the remaining sequences were verified using SMART (http://smart.embl-heidelberg.de) and Pfam (https://www.ebi.ac.uk/interpro/) tools. The physical and chemical properties of the identified GGPS family members, including amino acid count, molecular weight, and theoretical isoelectric points, were analyzed using BioPerl[21].

Phylogenetic analysis

Multiple sequence alignments of potato GGPS, along with GGPS sequences from Arabidopsis, tobacco, tomato (SlGGPS), and pepper, were performed using the MUSCLE algorithm. A phylogenetic tree was constructed using IQ-TREE with 1,000 bootstrap replicates [22].

Gene structure, conserved motifs, and 3D structural analysis

Gene structure information for potato GGPS family members was extracted from genome annotation files, and intron/exon structures were visualized using GSDS 2.0 (http://gsds.gao-lab.org/)[23]. Conserved motifs were identified using the MEME 5.5.5 online tool (http://meme-suite.org/) with the following parameters: a maximum number of 10 motifs, a motif width of 6-50, amino acids, and default settings for other parameters[24]. Subcellular location predictions were conducted using WoLF PSORT[25]. The three-dimensional structural models of potato GGPS genes were retrieved from the RCSB PDB database (https://www.rcsb.org/) and refined using PSI-BLAST, SWISS-MODEL (https://swissmodel.expasy.org/), and SAVES (https://saves.mbi.ucla.edu/) for quality evaluation[26, 27].

Analysis of cis-acting elements in promoter regions

The cis-acting elements within 2 kb upstream of the potato GGPS gene promoters [28] were analyzed using the PlantCARE database, and the elements were visualized using the GGPS 2.0 website (http://gsds.gao-lab.org/)[23].

Chromosomal location, gene distribution and synteny analysis

The chromosomal locations of StGGPS family members were extracted from genome annotation files and mapped using TBtools II[29]. Duplication events among potato GGPS genes were analyzed with MscanX software[30], and synteny relationships were visualized using Circos[31]. Synonymous substitution (Ks) and non-synonymous substitution (Ka) substitution rates for duplicated gene pair were calculated using KaKs Calculator 2.0[32]. Furthermore, MScanX software was used to analyze the collinearity between potato GGPS genes and multiple species.

Expression analysis of RNA data

RNA-seq data were obtained from NCBI to assess the expression pattern of GGPS genes in potato tubers of various colors (white, yellow, red, and purple) and under abiotic stresses, including salt stress (200 mM NaCl for 12 and 24 h) and simulated drought stress (150 mM mannitol for 12 and 24 h). A heat map of gene expression was generated using TBtools II[29].

Identification of GGPS gene family members and analysis of protein physicochemical properties in potatoes

Eleven GGPS (StGGPS) gene family members were identified in potatoes using HMMER 3.1 in conjunction with the SMART, Pfam, and NCBI CDD databases. The StGGPS genes were sequentially named (StGGPS1-StGGPS11). BioPerl analysis showed that the amino acid length of StGGPS family members ranges from 294 to 398 residues, with an average length of 351 residues. The molecular weight varies from 32,784.6 to 43,490.4 Da, with an average molecular weight of 38,973.8 Da. The theoretical isoelectric point ranges from 4.87 and 8.38, with an average of 6.41. Among the StGGPS genes, six are primarily localized in the chloroplast, two are found in the cytoplasm, nucleus, and mitochondria, and one is associated with the cytoskeleton (Table 1).

Table 1 Analysis of potato GGPS gene family members and physicochemical properties

Gene ID	Gene Name	Chromosome localization				Amino acid length(aa)	Molecular Weight(Da)	Theoretical isoelectric point	Subcellular localization
PGSC0003DMG400047044	StGGPS1	chr02	40939136	40940224	+	362	39321	6.35	Chloroplast
PGSC0003DMG400041508	StGGPS2	chr02	40941168	40942286	+	372	41120.1	8.38	Mitochondrion
PGSC0003DMG400043267	StGGPS3	chr02	40945073	40946191	+	372	40731.9	7.92	Chloroplast
PGSC0003DMG400027856	StGGPS4	chr04	69344146	69345467	-	375	40657.5	4.99	Chloroplast
PGSC0003DMG400007081	StGGPS5	chr07	52190753	52195395	-	398	43490.4	6.01	Chloroplast
PGSC0003DMG400022214	StGGPS6	chr07	54896132	54897257	-	294	32784.6	7.01	Cytoskeleton
PGSC0003DMG400002687	StGGPS7	chr09	4028005	4032971	+	334	36484.6	5.26	Chloroplast
PGSC0003DMG400008690	StGGPS8	chr10	854194	861002	+	342	39650.3	6.12	Cytoplasm
PGSC0003DMG400014369	StGGPS9	chr10	871271	879652	+	306	35198.2	6.77	Nucleus
PGSC0003DMG400015673	StGGPS10	chr11	1682159	1683721	-	365	39976.7	6.85	Chloroplast
PGSC0003DMG400029788	StGGPS11	chr12	10169940	10174778	-	342	39296.9	4.87	Cytoplasm

Potato GGPS family evolution analysis, gene structure and conserved motifs

To explore the evolution of the GGPS gene family, a phylogenic tree was constructed using genes from Arabidopsis (Arabidopsis thaliana), potato (Solanum tuberosum), tobacco (Nicotiana attenuata), tomato (Solanum lycopersicum), and hot pepper (Capsicum annuum) (Fig.1). The GGPS genes were divided into three subfamilies: Group 3, with seven potato StGGPS members; Group 2, with three potato StGGPS members; and Group 1, with one potato StGGPS member. Members within the same branch likely have similar functions and evolutionary relationships.

A better understanding of StGGPS evolutionary relationships between genes further analyzes the potato StGGPS member intron-explicit substructure and conservative motifs (Fig.1). The genetic structure of different StGGPS members varies; some genes do not contain introns, whereas others contain up to 11 introns. The diversity of the gene structures suggests that the StGGPS genes may have undergone different selection events during evolution. The StGGPS genes in the same subfamily generally had similar gene structures according to the phylogenetic tree, indicating that the intron-exon gene structure of the StGGPS genes was highly correlated with their phylogenetic relationships. The conserved base sequence is usually associated with the function of proteins, and MEME was used to identify 10 Motif (Motif1 ~ Motif10). The number of motifs per StGGPS member ranged from three to seven. For example, StGGPS5 contains a minimum of three motifs, whereas StGGPS2 and StGGPS3 contain a maximum of seven motifs. Although some motifs are missing in certain StGGPS members, all genes share a conserved pattern, particularly Motif3, which is highly conserved among the StGGPS genes. Analysis of the three-dimensional structures revealed that proteins within the same subfamily exhibit higher structural similarity compared to those across different subfamilies. For example, StGGPS8, StGGPS9, and StGGPS11 from Group 2 have similar structures, as do StGGPS1, StGGPS2, StGGPS3, StGGPS4, and StGGPS10 from Group3 (Fig.2). This combined analysis of the phylogenetic tree, gene structure, and conserved motifs suggests that StGGPS members within the same subfamily share similar gene functions and protein structures, indicating similar roles. We hypothesized that similar gene structures and conserved motifs in StGGPS would indicate similar functions and roles.

Fig.1 Phylogenetic, gene structure and conserved motif analysis of the GGPS gene family. A:Phylogenetic tree of the GGPS gene family in Arabidopsis_thaliana、Solanum_tuberosum、Nicotiana_attenuata、Solanum_lycopersicum、Capsicum_annuum.B: Phylogenetic tree of the StGGPS gene family.C: Conserved motif analysis of the StGGPS gene.D: Analysis of StGGPS gene structure.

Fig.2 Three-dimensional structural modeling of proteins of the StGGPS gene family.

Chromosome localization of genes and analysis of gene duplication events

StGGPS family members on the chromosome location information were extracted from the genome annotation file using Tbtools II. We found that chromosome 2 contained three StGGPS genes; chromosomes 7 and 10 contained two StGGPS genes; and chromosomes 4, 9, 11, and 12 contained only one StGGPS gene (Fig.3A).

To explore the structural and functional characteristics of the StGGPS genes, we examined gene duplications through tandem repeats and segmental duplications. We identified StGGPS gene pairs resulting from duplication events, specifically: StGGPS1: StGGPS4 (Fig.3B). We found three pairs of tandem repeat genes: StGGPS1, StGGPS2, StGGPS2, StGGPS3, StGGPS8, and StGGPS9. Gene duplication and fragment duplication likely drove the evolution of StGGPS genes. Further analysis of the Ka/Ks ratios for each pair indicated that the ratios ranged from 0.0634 (StGGPS1 / StGGPS4) to 0.6052 (StGGPS8 / StGGPS9), suggesting selective pressure on these genes.

To understand the evolutionary mechanisms of the potato GGPS family, we performed linear analysis using Arabidopsis and Solanaceae plants (tobacco, tomatoes, peppers, and potatoes) (Fig.3C). Four pairs of homologous genes were identified between potato and Arabidopsis thaliana. Two homologous pairs were found between potatoes and tobacco, eight homologous genes between potatoes and tomatoes, and seven between potatoes and peppers. These homologous genes likely existed before the divergence of ancestral lineages.

Fig.3 Gene duplication events in the GGPS family of S. tuberosum. A:Chromosomal localization map of StGGPS gene.B:Covariance analysis of StGGPS gene.C: Collinearity analysis of GGPS genes in multiple species.

Analysis of cis-acting elements in StGGPS gene promoters

To explore the potential functions of StGGPS genes, we analyzed the 2000 bp upstream promoter sequence. We identified 10 cis-acting elements (Fig.4) associated with various physiological processes. Notably, elements such as Box4, G-box, GATA-motif, GT1-motif, and TCT-motif, which are related to light sensing, were prevalent. This suggests that the StGGPS gene family is involved in potato photosynthesis. Additionally, StGGPS genes associated with abiotic stress responses contained cis-elements such as ABRE (involved in abscisic acid response) ARE (anaerobic response), CGTCA-motif and TGACG-motif (jasmonic acid response), and TGA (auxin response). Overall, StGGPS genes likely play significant roles in light and abiotic stress responses in potatoes.

Fig.4 Original analysis of the cis-acting 2000 bp promoter of the StGGPS gene.

Expression patterns of genes in tubers of different colors

Different colored potato tubers exhibit obvious differences in their carotenoid content[33]. To further investigate the expression of StGGPS in tubers of different colors, RNA-seq data were used to analyze the expression of StGGPS genes in potato blocks of the four different colors (Fig.5). Results indicated differential expression of StGGPS genes based on tuber color. In yellow tubers, StGGPS1, StGGPS3, StGGPS4, and StGGPS7 were upregulated. In white tubers, StGGPS2, StGGPS5, StGGPS8, and StGGPS9 showed increased expression. In red tubers, StGGPS6, StGGPS10, and StGGPS11 were upregulated, while in purple tubers, StGGPS gene expression was downregulated. This suggests that yellow and red tubers may have higher carotenoid content, while purple tubers may have lower carotenoid content and higher anthocyanin content compared to other tubers.

Fig.5 Expression of StGGPS gene in different colored tubers (P: purple potato; R: red potato; W: white potato; Y: yellow potato).

Gene expression patterns in response to abiotic stress

Abiotic stresses, such as drought and salt stress, significantly impact potato production. To investigate the response of the StGGPS family to these stresses, we analyzed RNA-seq data from NCBI, validated by RT-qPCR. Under drought stress, the RNA-seq data revealed differential expression of StGGPS genes. Specifically, StGGPS9 and StGGPS10 were upregulated, whereas other StGGPS members were downregulated. RT-qPCR verification confirmed that StGGPS10 was particularly sensitive to drought stress, suggesting it plays a critical role in enhancing drought resistance in potatoes(Fig.6). In response to salt stress, RNA-seq data indicated differential expression of several StGGPs, including StGGPS3, StGGPS4, StGGPS9, StGGPS10, StGGPS2, StGGPS5, StGGPS6, and StGGPS11. RT-qPCR results confirmed that StGGPS6 also responded to salt stress (Fig.7). Based on these findings, we hypothesize that StGGPS6 and StGGPS10 play important roles in the abiotic stress response of potatoes.

Fig.6 Expression of StGGPS gene under drought stress. A:Expression of StGGPS under drought stress.B:Relative expression of StGGPS under drought stress.

Fig.7 Expression of StGGPS gene under salt stress. A:Expression of StGGPS under salt stress.B:Relative expression of StGGPS under salt stress.

The StGGPS gene family in potatoes can be divided into three subfamilies, with Group 3 containing seven members, Group 2 containing two members, and Group 1 containing one member. The presence of ancient duplication events and the high retention rate of existing duplicate gene pairs has contributed to the emergence of numerous duplicate genes in the plant genome[34]. In this study, we identified a duplicate gene pair (StGGPS1/StGGPS4) within Group 3, indicating that this group plays a significant role in the expansion of the StGGPS gene family. Notably, RNA-seq data revealed that the expression patterns of the StGGPS1 and StGGPS4 genes in potato blocks of different colors, suggesting their involvement in the same pathway regulating potato carotenoid synthesis.

Furthermore, RNA-seq and RT-qPCR analyses confirmed that StGGPS1 was downregulated under drought stress conditions, whereas StGGPS4 was upregulated. In contrast, under salt stress conditions, StGGPS1 was upregulated, and StGGPS4 was downregulated. These findings suggest that StGGPS1 and StGGPS4 may have distinct roles in the potato plant’s response to abiotic stress. Additionally, our collinearity across species revealed that certain StGGPS genes are evolutionarily conserved. For instance, StGGPS7 (PGSC0003DMG400002687) in potatoes is homologous to NaGGPS2 (A4A49_09152) in tobacco, SlGGPS6 (Solyc09g008920.3) in tomato, and CaGGPS10 (T459_22463) in pepper. Additionally, StGGPS9 (PGSC0003DMG400014369) in potatoes was homologous to NaGGPS3 (A4A49_24015) in tobacco, SlGGPS8(Solyc10g005840.3) in tomatoes, and CaGGPS11(T459_24642) in pepper plants. These genes may have been present before the divergence of the ancestral lineages of Solanaceae, and at the same time these orthologous genes may play similar functions and roles in different Solanaceae species.

As a key enzyme in the synthesis of terpenoids, geranyl geranyl pyrophosphate synthase (GGPS) catalyzes the production of geranyl geranyl pyrophosphate (GGPP), a crucial compound in plant photosynthesis and biotic/abiotic stress responses[14, 15, 35]. Previous studies have demonstrated that NtGGPPS1 and NtPSY1 in tobacco form a multi-enzyme complex that regulates carotenoid biosynthesis and the co-expression of genes in the carotenoid biosynthesis pathway[35]. Similarly, ApGGPS is the key enzyme in andrographolide synthesis and plays a role in photosynthesis, growth, and other physiological processes in plants by participating in GGPP synthesis[36].

Through collinearity analysis, we identified four pairs of homologous genes in potato and Arabidopsis, including StGGPS2(PGSC0003DMG400041508), AtGGPS5(AT2G18640), AtGGPS15(AT4G36810), StGGPS5(PGSC0003DMG400007081), AtGGPS1(AT1G17050), and AtGGPS3(AT1G78510). AtGGPS15(AT4G36810), which is a key isoenzyme required for the production of most isoprene compounds involved in photosynthesis[33]. We hypothesize that StGGPS2 might have a similar function to AtGGPS15 and play a significant role in the photosynthetic reactions of potatoes. In addition, AtGGPS1(AT1G17050) and AtGGPS3(AT1G78510) are paralogous genes involved in the synthesis of the REDOX cofactor plastoquinine-9 in photosynthesis[37], a key antioxidant in plant leaves that plays a critical role in photoprotection[38]. Higher plastoquinin-9 activity in potatoes could enhance resistance to the effects of salt stress on photosynthesis[39]StGGPS5 is homologous to AtGGPS1(AT1G17050) and AtGGPS3(AT1G78510), and RNA-seq data show significant upregulation of StGGPS5 under salt stress, we propose that StGGPS5 may be closely related to plastoquinone-9 synthesis in potatoes and participate in their response to salt stress, thereby mitigating the adverse effects of salt on potato growth and development.

Eleven StGGPS family genes were identified and classified into three subfamilies based on gene structure and conserved motif analysis. Bioinformatics analysis and gene expression verification revealed that these genes contain numerous photo responsive and cis-acting elements related to abiotic stress responses. Combined with transcriptome data and q-PCR verification, our findings suggest that StGGPS family members play a significant role in helping potatoes resist damage caused by abiotic stress, thereby supporting the plant’s growth and development under adverse conditions.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request(PRJNA1064146 , PRJNA882516 and PRJNA646050).

Competing interests

The authors declare that they have no competing interests" in this section.

Funding

This work was supported by the Hebei Province modern agricultural industrial technology system tuber industry innovation team special & Hebei province detoxigenic potato breeding technology innovation center(HBCT2023060201 & SG2012016).

Authors’ contributions

Q.C. M. and W. L. conceived and designed experiments, and edited the manuscript. S.J. G. designed primers and performed the qRT-PCR.M.F. J. and X.T. C. checked the language specification of manuscript. S.Q.Z. and J.H. C. designed the experiment and reviewed the paper. All authors read and approved the final manuscript.

Acknowledgements

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Authors’ information

Hebei Agticultural University；Hebei Key Laboratory of Crop Germplasm Resources；North China Key Laboratory for Crop Germplasm Resources of Education Ministry.BaoDing, HeBei,China

Quancai Man,Wei Li,Shunjuan Gao and Jianghui Cui

Weichang county manchu and Mongolian autonomous county potato research institute,Wei Chang,HeBei,China

Xiaotian Chen

Shijiazhuang Academy of Agriculture and Forestry,ShiJiaZhuang,HeBei,China

Mingfei Jia and Shuqing Zhang

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No competing interests reported.

Genome-wide identification of the potato GGPS gene family and analysis of its response to abiotic stress

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Abstract

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Background

Materials and Methods

Results

Discussion

Conclusion

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Additional Declarations

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