Abstract
The Cullin-RING E3 ubiquitin ligase (CRL) complex is the most common E3 ligase, and the SCF complex (CRL1) has the most diverse functions. Cullin1(CUL1) is a scaffolding protein for assembly of the complex. SCF has been shown to participate in the non-biological stress response pathways. In this study, a classic CUL1 protein was identified in Solanum tuberosum, StCUL1. A full-length cDNA of the StCUL1 gene was obtained from ED13 (a potato variety) by Ralstonia solanacearum inoculation using the RACE method. Sequence analysis indicated that the gene comprised 2662 bp, with an open reading frame of 2229 bp encoding 743 amino acids. The expression levels of the StCUL1 gene in potato treated with R. solanacearum and exogenous hormones (such as salicylic acid, jasmonic acid methyl ester and abscisic acid) at different time points were determined by real-time PCR. The results indicated that StCUL1 was induced not only by pathogenic bacteria, but also by exogenous hormones, with sustained high expression. However, there were some differences in the modes of expression. Tissue localization analysis indicated that its expression was tissue specific, and it was mainly in the phloem of the vascular system of stems and leaves.
Similar content being viewed by others
Abbreviations
- CRL:
-
Cullin-RING E3 ubiquitin ligase
- UPS:
-
Ubiquitin–proteasome system
- HECT:
-
Homology to E6-AP Carboxyl Terminus
- cdc53:
-
Cell division control protein 53
- RBX1:
-
Ring-box 1
- SKP1:
-
Suppressor of kinetochore protein 1
- SLY1:
-
S-phase kinase-associated protein 1
- Max2:
-
MORE AXILLARY BRANCHES 2
References
An JP, Li R, Qu FJ et al (2016) Apple F-Box protein MdMAX2 regulates plant photomorphogenesis and stress response. Front Plant Sci 7:1685
Bornstein G, Ganoth D, Hershko A (2006) Regulation of neddylation and deneddylation of cullin1 in SCFSkp2 ubiquitin ligase by F-box protein and substrate. Proc Natl Acad Sci USA 103(31):11515–11520
Burg HAVD, Tsitsigiannis DI, Rowland O et al (2008) The F-Box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20(3):697–719
Cao Y, Yang Y, Zhang H et al (2008) Overexpression of a rice defense-related F-box protein gene OsDRF1 in tobacco improves disease resistance through potentiation of defense gene expression. Physiol Plant 134(3):440–452
Chen R, Guo W, Yin Y et al (2014) A novel F-box protein caf-box is involved in, responses to plant hormones and abiotic stress in pepper (Capsicum annuum L.). Int J Mol Sci 15(2):2413–2430
Chen Y, Chi Y, Meng Q et al (2018) GmSK1, a SKP1 homologue in soybean, is involved in the tolerance to salt and drought. Plant Physiol Biochem 127:25–31
Cheng C, Wang Z, Ren Z et al (2017) SCFatpp2-b11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet 13(8):e1006947
Christians MJ, Rottier A, Wiersma C (2018) Light regulates the rubylation levels of individual cullin proteins in Arabidopsis thaliana. Plant Mol Biol Rep 36(1):1–12
Do SI, Kim K, Lee H et al (2014) Aberrant expression pattern and location of cullin 1 are associated with the development of papillary carcinoma in thyroid and cyclin d1 expression. Endocr Pathol 25(3):282–287
Feng S, Ma L, Wang X et al (2003) The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 15(5):1083–1094
Feng S, Shen Y, Sullivan JA et al (2004) Arabidopsis CAND1, an unmodified CUL1-interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell 16(7):1870–1882
Gao G, Ren CH, Jin LP et al (2008) Cloning, expression and characterization of a nonspecific lipid transfer protein gene from potato. Acta Agron Sin 34(9):1510–1517
Gilkerson J, Hu J, Brown J et al (2009) Isolation and characterization of CUL1-7, a recessive allele of cullin1 that disrupts SCF function at the C terminus of cul1 in Arabidopsis thaliana. Genetics 181(3):945–963
Griffiths J, Murase K, Rieu I et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18(12):3399–3414
He LY (1983) Characteristics of strains of Pseudomonas solanacearum from China. Plant Dis 67(12):1357–1361
He Y, Wang C, Higgins J et al (2016) Meiotic F-box is essential for male meiotic DNA double strand break repair in rice. Plant Cell 28(8):1879–1893
Hellmann H, Hobbie L, Chapman A et al (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22(13):3314–3325
Hotton SK, Callis J (2008) Regulation of cullin-RING ligases. Annu Rev Plant Biol 59(1):467–489
Jain M, Kaur N, Tyagi AK et al (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genom 6(1):36–46
Jia F, Wang C, Huang J et al (2015) SCF E3 ligase pp 2–b11 plays a positive role in response to salt stress in Arabidopsis. J Exp Bot 66(15):4683–4697
Jiao L, Fu S, Zhang Y et al (2016) U-box E3 ubiquitin ligases regulate stress tolerance and growth of plants. Chin Bull Bot 57(6):1189–1209
Katsir L, Chung HS, Koo AJ et al (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11(4):428–435
Kim SH, Woo OG, Jang H et al (2018) Characterization and comparative expression analysis of CUL1 genes in rice. Genes Genom 40(3):1–9
Kipreos ET, Lander LE, Wing JP et al (1996) CUL-1, is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85(6):829–839
Lee JH, Kim WT (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31(3):201–208
Li Y, Jia F, Yu Y et al (2014) The SCF E3 ligase AtPP2-B11 plays a negative role in response to drought stress in Arabidopsis. Plant Mol Biol Rep 32(5):943–956
Li Y, Zhang L, Li D et al (2016) The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signaling by facilitating ABA receptor RCAR3 degradation. Plant Cell Environ 39(3):571–582
Li Q, Wang W, Wang W, Zhang G et al (2018) Wheat F-box protein gene TaFBA1is involved in plant tolerance to heat stress. Front Plant Sci 9:521
Magori S, Citovsky V (2011) Hijacking of the host SCF ubiquitin ligase machinery by plant pathogens. Front Plant Sci 2:87
Maldonado-Calderón MT, Sepúlveda-García E, Rocha-Sosa M (2012) Characterization of novel F-box proteins in plants induced by biotic and abiotic stress. Plant Sci 185–186(4):208–217
Ni X, Tian Z, Liu J et al (2010) StPUB17, a novel potato UND/PUB/ARM repeat type gene, is associated with late blight resistance and NaCl stress. Plant Sci 178(2):158–169
Pauwels L, Ritter A, Goossens J et al (2015) The RING E3 ligase KEEP ON GOING modulates JASMONATE ZIM-DOMAIN12 stability. Plant Physiol 169(2):1405–1417
Pieterse CM, Leonreyes A, Van DES et al (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316
Piisilä M, Keceli MA, Brader G et al (2015) The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol 15(1):53
Prakash C, Manjrekar J, Chattoo BB (2016) Skp1, a component of E3 ubiquitin ligase, is necessary for growth, sporulation, development and pathogenicity in rice blast fungus (Magnaporthe oryzae). Mol Plant Pathol 17(6):903–919
Ren C, Pan J, Peng W et al (2010) Point mutations in Arabidopsis cullin1 reveal its essential role in jasmonate response. Plant J 42(4):514–524
Robert-Seilaniantz A, Grant M, Jones JDG (2010) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49(1):317–343
Sadanandom A, Bailey M, Ewan R et al (2012) The ubiquitin–proteasome system: central modifier of plant signalling. New Phytol 196(1):13–28
Salanoubat M, Genin S, Artiguenave F et al (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415(6871):497–502
Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12(1):57–62
Shen WH, Parmentier Y, Hellmann H et al (2002) Null mutation of atcul1 causes arrest in early embryogenesis in Arabidopsis. Mol Biol Cell 13(6):1916–1928
Song S, Dai X, Zhang WH (2012) A rice F-box gene, OsFBX352, is involved in glucose-delayed seed germination in rice. J Exp Bot 63(15):5559–5568
Stratmann JW, Gusmaroli G (2012) Many jobs for one good cop the COP9 signalosome guards development and defense. Plant Sci 185–186(4):50–64
Tao T, Zhou CJ, Wang Q et al (2017) Rice black streaked dwarf virus P7-2 forms a SCF complex through binding to Oryza sativa SKP1-like proteins, and interacts with GID2 involved in the gibberellin pathway. PLoS ONE 12(5):e0177518
Thomas S, Kenneth D, Livak J (2008) Analyzing real-time PCR data by comparative C(T) method. Nat Protoc 3(6):1101–1108
Wang J, Yao W, Wang L et al (2017) Overexpression of VpEIFP1, a novel F-box/Kelch-repeat protein from wild Chinese Vitis pseudoreticulata, confers higher tolerance to powdery mildew by inducing thioredoxin z proteolysis. Plant Sci 263:142–155
Zanati OEL, Roche J, Boulaflous-Stevens A et al (2017) Genome-wide analysis, classification, expression and interaction of physcomitrella patens SKP1-like, (PpSKP) and F-box (FBX) genes. Plant Gene 12:13–22
Zhang Y, Xu W, Li Z et al (2009) F-box protein dor functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148(5):2121–2133
Zhang Y, Wang C, Lin Q et al (2015) Genome-wide analysis of phylogeny, expression profile and sub-cellular localization of skp1-like genes in wild tomato. Plant Sci 238:105–114
Zheng N, Schulman BA, Song L et al (2002) Structure of the Cul1-Rbx1-skp1-Fboxskp2 SCF ubiquitin ligase complex. Nature 416:703–709
Zhou SM, Kong XZ, Kang HH et al (2015) The involvement of wheat F-box protein gene TaFBA1 in the oxidative stress tolerance of plants. PLoS ONE 10(4):e0122117
Acknowledgements
We would like to thank the institutes of Vegetables and Flowers and Plant Protection of the Chinese Academy of Agricultural Sciences for potato materials. This work was supported by the project of National Natural Science Foundation of China (31771858).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No conflict of interest was declared.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
13562_2019_495_MOESM1_ESM.tif
Supplementary Figure 1 StCUL1 shares high structural similarity in different species. A Protein sequence alignment of StCUL1 showing the conserved domains. The amino acid sequence of StCUL1 was aligned with Solanum lycopersicum (XP_004229226.1), Capsicum annuum (XP_016542284.1), Nicotiana sylvestris (XP_009780619.1), and Petunia hybrida (BAW00386.1) homologs. The Cullin domain, consisting of 150 (418-567) amino acid residues and the cullin-nedd8 domain, consisting of 68 (669-736) amino acid residues, are represented by a solid line, which is conserved across many species. The comparison software was performed using DNAMAN6.0 software. Black indicates 100% conservatism, dark gray shading indicates 70% conservatism, and light gray shading indicates 50% conservatism. B A phylogenetic tree was generated from a multiple sequence alignment using Neighbour-Joining method with 1000 bootstrap replicates by MEGA 5 software. (TIFF 26184 kb)
13562_2019_495_MOESM2_ESM.tif
Supplementary Figure 2 Structure representation of StCUL1 protein predicted using the PSIPRED Web Server (http://bioinf.cs.ucl.ac.uk/psipred/). A Secondary structure showing alpha helix、extended strand、beta-turn and random coil. B Ribbon representation of the 3D structure of StCUL1 modified on SWISS Web Server (https://swissmodel.expasy.org/). (TIFF 5860 kb)
13562_2019_495_MOESM3_ESM.tif
Supplementary Figure 3 Cis-acting regulatory elements in the promoter regions of StCUL1. The 1572 bp upstream of the start codon was analyzed based on the PLACE, PlantCARE and potato genome sequence databases from GenBank (https://www.ncbi.nlm.nih.gov/). Different cis-elements showed by colored squares. (TIFF 6424 kb)
Rights and permissions
About this article
Cite this article
Pang, PX., Shi, L., Wang, XJ. et al. Cloning and expression analysis of the StCUL1 gene in potato. J. Plant Biochem. Biotechnol. 28, 460–469 (2019). https://doi.org/10.1007/s13562-019-00495-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-019-00495-2