Abstract
Ubiquitin-mediated proteolysis is a central pathway that controls protein turnover. Ubiquitin–proteasome pathway works sequentially to ubiquitinate appropriate substrates that subsequently lead to its degradation via 26S proteasome. Among the several classes of ubiquitin E3 ligases, the SKP1-Cullin-F-box class is generally the most common and widely explored. SKP1-like proteins in plants have gained less attention than other SCF complex components, although they have a larger involvement in controlling wide aspects of vascular plants. Several studies have shown that SKP1-like proteins regulate abiotic stress tolerance on their own, in addition to working in the SCF complex. However, the identification and characterization of SKP1-like genes in chickpea are missing. In the present study, we have identified 15 SKP1-like genes in the chickpea genome that have been categorized into three types type Ia, type Ib, and type II based on the structure and sequence. The evolutionary conservation of the chickpea SKP1 family with dicots and monocots was discovered utilizing phylogenetic analysis. The presence of hormone, plant growth and development, and various stress-related cis-regulatory elements in all chickpea SKP1-like gene promoters showed that SKP1-like genes have a potential role in functions in hormone and various abiotic stress signaling in chickpea. According to the qRT-PCR expression study, most chickpea SKP1-like genes are differently expressed under three abiotic stresses; namely drought, salt, and oxidative stress. As a result, the current work offers up new possibilities for leveraging SKP1-related data to better understand the role of abiotic stress tolerance in the chickpea plant.
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References
Abd-Hamid NA, Ahmad-Fauzi MI, Zainal Z, Ismail I (2020) Diverse and dynamic roles of F-box proteins in plant biology. Planta 251:68
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49. https://doi.org/10.1093/NAR/GKV416
Bryman A, Cramer D (2012) Quantitative data analysis with IBM SPSS 17, 18 & 19: a guide for social scientists. Quant Data Anal with IBM SPSS 17(18):19. https://doi.org/10.4324/9780203180990
Chang B, Partha S, Hofmann K et al (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263–274. https://doi.org/10.1016/S0092-8674(00)80098-7
Connelly C, Hieter P (1996) Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86:275–285. https://doi.org/10.1016/S0092-8674(00)80099-9
Farrás R, Ferrando A, Jásik J et al (2001) SKP1–SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 20:2742–2756. https://doi.org/10.1093/EMBOJ/20.11.2742
Gagne JM, Downes BP, Shiu SH et al (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99:11519–11524. https://doi.org/10.1073/pnas.162339999
George D, Mallery P (2019) IBM SPSS Statistics 26 Step by Step: a simple guide and reference. IBM SPSS Stat 26 Step by Step. https://doi.org/10.4324/9780429056765
Hao Q, Ren H, Zhu J et al (2016) Overexpression of PSK1, a SKP1-like gene homologue, from Paeonia suffruticosa, confers salinity tolerance in Arabidopsis. Plant Cell Rep 361(36):151–162. https://doi.org/10.1007/S00299-016-2066-Z
He Y, Wang C, Higgins JD et al (2016) MEIOTIC F-BOX is essential for male meiotic DNA double-strand break repair in rice. Plant Cell 28:1879–1893. https://doi.org/10.1105/tpc.16.00108
Hershko A, Ciechanover A (2003) The Ubiquitin system. Annu Rev Biochem 67:425–479. https://doi.org/10.1146/ANNUREV.BIOCHEM.67.1.425
Hu B, Jin J, Guo A-Y et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296. https://doi.org/10.1093/BIOINFORMATICS/BTU817
Kahloul S, HajSalah El Beji I, Boulaflous A et al (2013) Structural, expression and interaction analysis of rice SKP1-like genes. DNA Res 20:67–78. https://doi.org/10.1093/DNARES/DSS034
Kong H, Leebens-Mack J, Ni W et al (2004) Highly heterogeneous rates of evolution in the SKP1 gene family in plants and animals: functional and evolutionary implications. Mol Biol Evol 21:117–128. https://doi.org/10.1093/MOLBEV/MSH001
Kong H, Landherr LL, Frohlich MW et al (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885. https://doi.org/10.1111/J.1365-313X.2007.03097.X
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/MOLBEV/MSY096
Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/NAR/30.1.325
Li M, Tang D, Wang K et al (2011) Mutations in the F-box gene LARGER PANICLE improve the panicle architecture and enhance the grain yield in rice. Plant Biotechnol J 9:1002–1013. https://doi.org/10.1111/J.1467-7652.2011.00610.X
Li C, Liu Z, Zhang Q et al (2012) SKP1 is involved in abscisic acid signalling to regulate seed germination, stomatal opening and root growth in Arabidopsis thaliana. Plant Cell Environ 35:952–965. https://doi.org/10.1111/J.1365-3040.2011.02464.X
Liu F, Ni W, Griffith ME et al (2004) The ASK1 and ASK2 genes are essential for Arabidopsis early development. Plant Cell 16:5–20. https://doi.org/10.1105/TPC.017772
Liu A, Yu Y, Duan X et al (2015) GsSKP21, a Glycine soja S-phase kinase-associated protein, mediates the regulation of plant alkaline tolerance and ABA sensitivity. Plant Mol Biol 87:111–124. https://doi.org/10.1007/S11103-014-0264-Z/FIGURES/8
Matsumoto D, Yamane H, Abe K, Tao R (2012) Identification of a Skp1-like protein interacting with SFB, the pollen S determinant of the gametophytic self-incompatibility in Prunus. Plant Physiol 159:1252–1262. https://doi.org/10.1104/pp.112.197343
Mistry J, Chuguransky S, Williams L et al (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49:D412–D419. https://doi.org/10.1093/NAR/GKAA913
Rao V, Petla BP, Verma P et al (2018) Arabidopsis SKP1-like protein13 (ASK13) positively regulates seed germination and seedling growth under abiotic stress. J Exp Bot 69:3899–3915. https://doi.org/10.1093/JXB/ERY191
Sagar S, Biswas DK, Singh A (2020) Genomic and expression analysis indicate the involvement of phospholipase C family in abiotic stress signaling in chickpea (Cicer arietinum). Gene 753:144797. https://doi.org/10.1016/J.GENE.2020.144797
Salvi P, Saxena SC, Petla BP et al (2016) Differentially expressed galactinol synthase(s) in chickpea are implicated in seed vigor and longevity by limiting the age induced ROS accumulation. Sci Rep 61(6):1–15. https://doi.org/10.1038/srep35088
Schulman BA, Carrano AC, Jeffrey PD et al (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2 complex. Nature 4086810(408):381–386. https://doi.org/10.1038/35042620
Seol JH, Shevchenko A, Shevchenko A, Deshaies RJ (2001) Skp1 forms multiple protein complexes, including RAVE, a regulator of V-ATPase assembly. Nat Cell Biol 34(3):384–391. https://doi.org/10.1038/35070067
Singh P, Kot R, Singh G, Kumar S (2003) A quick method to isolate RNA from wheat and other carbohydrate-rich seeds. Plant Mol Biol Reptr 21:93a
Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590
Takahashi N, Kuroda H, Kuromori T et al (2004) Expression and interaction analysis of Arabidopsis Skp1-related genes. Plant Cell Physiol 45:83–91. https://doi.org/10.1093/PCP/PCH009
Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient Aneuploids. Plant Cell 15:2192–2202. https://doi.org/10.1105/TPC.014019
Varshney RK, Hiremath PJ, Lekha P et al (2009) A comprehensive resource of drought- and salinity- responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC Genomics 10:1–18. https://doi.org/10.1186/1471-2164-10-523
Verma M, Kumar V, Patel RK et al (2015) CTDB: an integrated chickpea transcriptome database for functional and applied genomics. PLoS ONE 10:e0136880. https://doi.org/10.1371/JOURNAL.PONE.0136880
Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397
Weber H, Bernhardt A, Dieterle M et al (2005) Arabidopsis AtCUL3a and AtCUL3b form complexes with members of the BTB/POZ-MATH protein family. Plant Physiol 137:83–93. https://doi.org/10.1104/PP.104.052654
Yang M, Hu Y, Lodhi M et al (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc Natl Acad Sci USA 96:11416–11421. https://doi.org/10.1073/pnas.96.20.11416
Zhao D, Ni W, Feng B et al (2003) Members of the Arabidopsis-SKP1-like gene family exhibit a variety of expression patterns and may play diverse roles in Arabidopsis. Plant Physiol 133:203–217. https://doi.org/10.1104/PP.103.024703
Zheng F, Wu H, Zhang R et al (2016) Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics 171(17):1–13. https://doi.org/10.1186/S12864-016-2736-9
Acknowledgements
This work was supported by the core grant of the National Institute of Plant Genome Research (NIPGR). We would like to thank Dr. Jawahar Singh, Ms. Sushma Sagar, Dr. Roshan Singh, and Mr. Ajeet Singh (NIPGR) to help in troubleshooting. We would also like to thank the Council of Scientific and Industrial Research (CSIR) and University Grant Commission (UGC), Government of India, for research fellowships. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to e-resources.
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MM and VV conceptualized the idea of the article. VV has done all bioinformatics analyses, and experiments and wrote the first draft of the manuscript. AH designed qRT-PCR primers and help in stress treatment and sample collection. MM, VV, and AH read and approved the final manuscript.
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344_2022_10777_MOESM2_ESM.xlsx
Supplementary Table 2: Protein sequence alignment of Arabidopsis thaliana, Oryza sativa, Medicago truncatula, Glycine max, and Cicer arietinum SKP1-like genes by using MUSCLE. (XLSX 4942 kb)
344_2022_10777_MOESM5_ESM.xlsx
Supplementary Table 5: RPKM values obtained from Chickpea Transcriptome Database (CTDB) for the transcript of CaSKP genes. (XLSX 12 kb)
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Varshney, V., Hazra, A. & Majee, M. Identification, Genomic Organization, and Comprehensive Expression Analysis Reveals the Implication of Cicer arietinum SKP1-like Genes in Abiotic Stress. J Plant Growth Regul 42, 6074–6090 (2023). https://doi.org/10.1007/s00344-022-10777-0
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DOI: https://doi.org/10.1007/s00344-022-10777-0