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Plant function and evolutionary biology
RESEARCH ARTICLE

Identification and expression analysis of SBP-Box-like (SPL) gene family disclose their contribution to abiotic stress and flower budding in pigeon pea (Cajanus cajan)

Tayyaba Shaheen A , Abdul Rehman https://orcid.org/0000-0002-2408-0725 A , Amany H. A. Abeed B , Muhammad Waqas A , Asad Aslam C , Farrukh Azeem https://orcid.org/0000-0002-2702-0330 A * , Muhammad Qasim A , Muhammad Afzal A , Muhammad Farooq Azhar D , Kotb A. Attia https://orcid.org/0000-0002-2992-1765 E , Asmaa M. Abushady F G , Sezai Ercisli H and Nazia Nahid https://orcid.org/0000-0002-2075-3902 A *
+ Author Affiliations
- Author Affiliations

A Department of Bioinformatics and Biotechnology, Government College University, Faisalabad 38000, Pakistan.

B Department of Botany and Microbiology, Faculty of Science, Assiut University, Assiut 71516, Egypt.

C Key Laboratory for Sustainable Forest Ecosystem Management – Ministry of Education, College of Forestry, Northeast Forestry University, Harbin 150040, China.

D Department of Forestry and Range Management, Faculty of Agricultural Sciences and Technology, Bahauddin Zakaria University, Multan 60800, Pakistan.

E Department of Biochemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh, Riyadh 11451, Saudi Arabia.

F Biotechnology School, Nile University, 26th July Corridor, Sheikh Zayed City, Giza 12588, Egypt.

G Department of Genetics, Agriculture College, Ain Shams University, Cairo, Egypt.

H Department of Horticulture, Faculty of Agriculture, Ataturk University, Erzurum 25240, Turkey.


Handling Editor: Sajid Fiaz

Functional Plant Biology 51, FP23237 https://doi.org/10.1071/FP23237
Submitted: 9 October 2023  Accepted: 25 December 2023  Published: 15 February 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The SPL gene family (for Squamosa Promoter-binding like Proteins) represents specific transcription factors that have significant roles in abiotic stress tolerance, development and the growth processes of different plants, including initiation of the leaf, branching and development of shoot and fruits. The SPL gene family has been studied in different plant species; however, its role is not yet fully explored in pigeon pea (Cajanus cajan). In the present study, 11 members of the CcSPL gene family were identified in C. cajan. The identified SPLs were classified into nine groups based on a phylogenetic analysis involving SPL protein sequences from C. cajan, Arabidopsis thaliana, Cicer arietinum, Glycine max, Phaseolus vulgaris, Vigna unguiculata and Arachis hypogaea. Further, the identification of gene structure, motif analysis, domain analysis and presence of cis-regulatory elements in the SPL family members were studied. Based on RNA-sequencing data, gene expression analysis was performed, revealing that CcSPL2.1, 3 and 13A were significantly upregulated for salt-tolerance and CcSPL14 and 15 were upregulated in a salt-susceptible cultivar. Real-time qPCR validation indicated that CcSPL3, 4, 6 and 13A were upregulated under salt stress conditions. Therefore, molecular docking was performed against the proteins of two highly expressed genes (CcSPL3 and CcSPL14) with three ligands: abscisic acid, gibberellic acid and indole-3-acetic acid. Afterward, their binding affinity was obtained and three-dimensional structures were predicted. In the future, our study may open avenues for harnessing CcSPL genes in pigeon pea for enhanced abiotic stress resistance and developmental traits.

Keywords: bioinformatics, genome-wide analysis, molecular docking, molecular interaction analysis, next-generation sequencing, omics data analysis, plant hormone, salinity stress, structure prediction.

References

Abeed AHA, Dawood MFA (2020) Comparative impact of different iso-osmotic solutions on osmotic adjustment in Gossypium barbadense. Global NEST Journal 22, 75-84.
| Crossref | Google Scholar |

Abeed AHA, Ali M, Ali EF, Majrashi A, Eissa MA (2021) Induction of Catharanthus roseus secondary metabolites when Calotropis procera was used as bio-stimulant. Plants 10, 1623.
| Crossref | Google Scholar | PubMed |

Ahmed S, Rashid MAR, Zafar SA, Azhar MT, Waqas M, Uzair M, et al. (2021) Genome-wide investigation and expression analysis of APETALA-2 transcription factor subfamily reveals its evolution, expansion and regulatory role in abiotic stress responses in Indica Rice (Oryza sativa L. ssp. indica). Genomics 113, 1029-1043.
| Crossref | Google Scholar | PubMed |

Ahmed T, Masood HA, Noman M, AL-Huqail AA, Alghanem SMS, Khan MM, Muhammad S, Manzoor N, Rizwan M, Qi X, Abeed AHA, Li B (2023) Biogenic silicon nanoparticles mitigate cadmium (Cd) toxicity in rapeseed (Brassica napus L.) by modulating the cellular oxidative stress metabolism and reducing Cd translocation. Journal of Hazardous Materials 459, 132070.
| Crossref | Google Scholar | PubMed |

Ali MA, Azeem F, Nawaz MA, Acet T, Abbas A, Imran QM, et al. (2018) Transcription factors WRKY11 and WRKY17 are involved in abiotic stress responses in Arabidopsis. Journal of Plant Physiology 226, 12-21.
| Crossref | Google Scholar | PubMed |

Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Research 43, W39-W49.
| Crossref | Google Scholar | PubMed |

Brogan IJ, Khan N, Isaac K, Hutchinson JA, Pravica V, Hutchinson IV (1999) Novel polymorphisms in the promoter and 5′ UTR regions of the human vascular endothelial growth factor gene. Human Immunology 60, 1245-1249.
| Crossref | Google Scholar | PubMed |

Bultan T, Yu F, Alkhalaf M, Aydin A (2017) ‘String analysis for software verification and security.’ (Springer International Publishing: Cham, Switzerland)

Cao R, Guo L, Ma M, Zhang W, Liu X, Zhao H (2019) Identification and functional characterization of Squamosa promoter binding protein-like gene TaSPL16 in wheat (Triticum aestivum L.). Frontiers in Plant Science 10, 212.
| Crossref | Google Scholar |

Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237, 91-104.
| Crossref | Google Scholar | PubMed |

Chao L-M, Liu Y-Q, Chen D-Y, Xue X-Y, Mao Y-B, Chen X-Y (2017) Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage. Molecular Plant 10, 735-748.
| Crossref | Google Scholar | PubMed |

Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194-1202.
| Crossref | Google Scholar | PubMed |

Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Research 14, 1188-1190.
| Crossref | Google Scholar | PubMed |

Cui N, Sun X, Sun M, Jia B, Duanmu H, Lv D, et al. (2015) Overexpression of OsmiR156k leads to reduced tolerance to cold stress in rice (Oryza Sativa). Molecular Breeding 35, 214.
| Crossref | Google Scholar |

Dar WD (2009) ICRISAT surging ahead with innovations: a compendium of speeches and presentations. ICRISAT, International Crops Research Institute for the Semi-Arid Tropics. Available at https://oar.icrisat.org/1358/

Goddard TD, Huang CC, Ferrin TE (2005) Software extensions to UCSF chimera for interactive visualization of large molecular assemblies. Structure 13, 473-482.
| Crossref | Google Scholar | PubMed |

Halim SA, Waqas M, Khan A, Al-Harrasi A (2021) In silico prediction of novel inhibitors of SARS-CoV-2 main protease through structure-based virtual screening and molecular dynamic simulation. Pharmaceuticals 14, 896.
| Crossref | Google Scholar | PubMed |

Hanafy MS, El-Banna A, Schumacher HM, Jacobsen H-J, Hassan FS (2013) Enhanced tolerance to drought and salt stresses in transgenic faba bean (Vicia faba L.) plants by heterologous expression of the PR10a gene from potato. Plant Cell Reports 32, 663-674.
| Crossref | Google Scholar | PubMed |

Hou H, Li J, Gao M, Singer SD, Wang H, Mao L, et al. (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. PLoS ONE 8, e59358.
| Crossref | Google Scholar | PubMed |

Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296-1297.
| Crossref | Google Scholar | PubMed |

Ioannidi E, Rigas S, Tsitsekian D, Daras G, Alatzas A, Makris A, et al. (2016) Trichome patterning control involves TTG1 interaction with SPL transcription factors. Plant Molecular Biology 92, 675-687.
| Crossref | Google Scholar | PubMed |

Jorgensen SA, Preston JC (2014) Differential SPL gene expression patterns reveal candidate genes underlying flowering time and architectural differences in Mimulus and Arabidopsis. Molecular Phylogenetics and Evolution 73, 129-139.
| Crossref | Google Scholar | PubMed |

Jung J-H, Lee H-J, Ryu JY, Park C-M (2016) SPL3/4/5 integrate developmental aging and photoperiodic signals into the FT-FD module in Arabidopsis flowering. Molecular Plant 9, 1647-1659.
| Crossref | Google Scholar | PubMed |

Kim S, Chen J, Cheng T, Gindulyte A, He J, He S, et al. (2019) PubChem 2019 update: improved access to chemical data. Nucleic Acids Research 47, D1102-D1109.
| Crossref | Google Scholar | PubMed |

Kropat J, Tottey S, Birkenbihl RP, Depège N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proceedings of the National Academy of Sciences 102, 18730-18735.
| Crossref | Google Scholar |

Lei M, Li Z-Y, Wang J-B, Fu Y-L, Ao M-F, Xu L (2018) Constitutive expression of Aechmea fasciata SPL14 (AfSPL14) accelerates flowering and changes the plant architecture in Arabidopsis. International Journal of Molecular Sciences 19, 2085.
| Crossref | Google Scholar | PubMed |

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, 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 Research 30, 325-327.
| Crossref | Google Scholar | PubMed |

Li X-Y, Lin E-P, Huang H-H, Niu M-Y, Tong Z-K, Zhang J-H (2018) Molecular Characterization of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Gene Family in Betula luminifera. Frontiers in Plant Science 9, 608.
| Crossref | Google Scholar |

Ling L-Z, Zhang S-D (2012) Exploring the evolutionary differences of SBP-box genes targeted by miR156 and miR529 in plants. Genetica 140, 317-324.
| Crossref | Google Scholar | PubMed |

Liu M, Sun W, Ma Z, Huang L, Wu Q, Tang Z, et al. (2019) Genome-wide identification of the SPL gene family in Tartary Buckwheat (Fagopyrum tataricum) and expression analysis during fruit development stages. BMC Plant Biology 19, 299.
| Crossref | Google Scholar |

Mao H-D, Yu L-J, Li Z-J, Yan Y, Han R, Liu H, et al. (2016) Genome-wide analysis of the SPL family transcription factors and their responses to abiotic stresses in maize. Plant Gene 6, 1-12.
| Crossref | Google Scholar |

Mongkolsiriwatana C, Pongtongkam P, Peyachoknagul S (2009) In silico promoter analysis of photoperiod-responsive genes identified by DNA microarray in rice (Oryza sativa L.). Agriculture and Natural Resources 43, 164-177.
| Google Scholar |

Nadeem M, Khan AA, Nadeem J, Khan AA, Fatima U (2023) Cloning and characterization of Trichoderma glucanase gene for plant transformation. International Journal of Agriculture and Biosciences 12(1), 31-46.
| Crossref | Google Scholar |

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268-274.
| Crossref | Google Scholar | PubMed |

Noman MU, Azhar S (2023) Metabolomics, a potential way to improve abiotic stresses tolerance in cereal crops. International Journal of Agriculture and Biosciences 12(1), 47-55.
| Crossref | Google Scholar |

Palmeri D, Malim MH (1999) Importin β can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin α. Molecular and Cellular Biology 19, 1218-1225.
| Crossref | Google Scholar | PubMed |

Pasquier J, Cabau C, Nguyen T, Jouanno E, Severac D, Braasch I, et al. (2016) Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genomics 17, 368.
| Crossref | Google Scholar |

Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Frontiers in Plant Science 4, 80.
| Crossref | Google Scholar |

Rehman I, Shaukat F, Anwar Z, Ijaz A, Nadeem R (2022) Applications of Crispr/Cas system in plants. International Journal of Agriculture and Biosciences 11(4), 231-237.
| Crossref | Google Scholar |

Sherry ST, Ward M-H, Kholodov M, Baker J, Phan L, Smigielski EM, et al. (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Research 29, 308-311.
| Crossref | Google Scholar | PubMed |

Stief A, Altmann S, Hoffmann K, Pant BD, Scheible W-R, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. The Plant Cell 26, 1792-1807.
| Crossref | Google Scholar | PubMed |

Sun H, Mei J, Zhao W, Hou W, Zhang Y, Xu T, et al. (2022) Phylogenetic analysis of the SQUAMOSA promoter-binding protein-like genes in four Ipomoea species and expression profiling of the IbSPLs during storage root development in sweet potato (Ipomoea batatas). Frontiers in Plant Science 12, 801061.
| Crossref | Google Scholar |

Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, et al. (2007) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Research 36, D1009-D1014.
| Crossref | Google Scholar | PubMed |

Takahashi H, Fujishima T, Koba H, Murakami S, Kurokawa K, Shibuya Y, et al. (2000) Serum surfactant proteins A and D as prognostic factors in idiopathic pulmonary fibrosis and their relationship to disease extent. American Journal of Respiratory and Critical Care Medicine 162, 1109-1114.
| Crossref | Google Scholar | PubMed |

The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Research 43, D204-D212.
| Crossref | Google Scholar |

Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, et al. (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nature Biotechnology 30, 83-89.
| Crossref | Google Scholar |

Wang W (2015) The molecular detection of Corynespora Cassiicola on cucumber by PCR assay using DNAman software and NCBI. In ‘International conference on computer and computing technologies in agriculture’, pp. 248–258. (Springer)

Waqas M, Azhar MT, Rana IA, Azeem F, Ali MA, Nawaz MA, et al. (2019) Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea (Cicer arietinum L.) reveal their role in abiotic stress-responses. Genes & Genomics 41, 467-481.
| Crossref | Google Scholar | PubMed |

Waqas M, Haider A, Rehman A, Qasim M, Umar A, Sufyan M, et al. (2021) Immunoinformatics and molecular docking studies predicted potential multiepitope-based peptide vaccine and novel compounds against novel SARS-CoV-2 through virtual screening. BioMed Research International 2021, 1596834.
| Crossref | Google Scholar |

Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133, 3539-3547.
| Crossref | Google Scholar | PubMed |

Wu G, Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759.
| Crossref | Google Scholar | PubMed |

Xu Y, Xu H, Wall MM, Yang J (2020) Roles of transcription factor SQUAMOSA promoter binding protein-like gene family in papaya (Carica papaya) development and ripening. Genomics 112, 2734-2747.
| Crossref | Google Scholar | PubMed |

Xue X-Y, Zhao B, Chao L-M, Chen D-Y, Cui W-R, Mao Y-B, et al. (2014) Interaction between two timing microRNAs controls trichome distribution in Arabidopsis. PLoS Genetics 10, e1004266.
| Crossref | Google Scholar | PubMed |

Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends in Plant Science 10, 88-94.
| Crossref | Google Scholar | PubMed |

Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407, 1-11.
| Crossref | Google Scholar | PubMed |

Yu N, Cai W-J, Wang S, Shan C-M, Wang L-J, Chen X-Y (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. The Plant Cell 22, 2322-2335.
| Crossref | Google Scholar | PubMed |

Yu P, Shinde H, Dudhate A, Tsugama D, Gupta SK, Liu S, et al. (2021) Genome-wide investigation of SQUAMOSA promoter binding protein-like transcription factor family in pearl millet (Pennisetum glaucum (L) R. Br.). Plant Gene 27, 100313.
| Crossref | Google Scholar |

Zhang X, Dou L, Pang C, Song M, Wei H, Fan S, et al. (2015) Genomic organization, differential expression, and functional analysis of the SPL gene family in Gossypium hirsutum. Molecular Genetics and Genomics 290, 115-126.
| Crossref | Google Scholar | PubMed |

Zhong H, Kong W, Gong Z, Fang X, Deng X, Liu C, et al. (2019) Evolutionary analyses reveal diverged patterns of SQUAMOSA promoter binding protein-like (SPL) gene family in Oryza genus. Frontiers in Plant Science 10, 565.
| Crossref | Google Scholar |