Abstract
Main conclusion
SR proteins from sweet potato have conserved functional domains and similar gene structures as that of Arabidopsis and rice in general. However, expression patterns and alternative splicing regulations of SR genes from different species have changed under stresses. Novel alternative splicing regulations were found in sweet potato SR genes.
Abstract
Serine/arginine-rich (SR) proteins play important roles in plant development and stress response by regulating the pre-mRNA splicing process. However, SR proteins have not been identified so far from an important crop sweet potato. Through bioinformatics analysis, our study identified 24 SR proteins from sweet potato, with comprehensively analyzing of protein characteristics, gene structure, chromosome localization, and cis-acting elements in promotors. Salt, heat, and mimic drought stresses triggered extensive but different expressional regulations on sweet potato SR genes. Interestingly, heat stress caused the most active disturbances in both gene transcription and pre-mRNA alternative splicing (AS). Tissue and species-specific transcriptional and pre-mRNA AS regulations in response to stresses were found in sweet potato, in comparison with Arabidopsis and rice. Moreover, novel patterns of pre-mRNA alternative splicing were found in SR proteins from sweet potato. Our study provided an insight into similarities and differences of SR proteins in different plant species from gene sequences to gene structures and stress responses, indicating SR proteins may regulate their downstream genes differently between different species and tissues by varied transcriptional and pre-mRNA AS regulations.
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Data availability
All main data of the study appear in the submitted article. Supplementary data are available at Planta online.
Change history
20 September 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00425-022-04000-3
Abbreviations
- AS:
-
Alternative splicing
- ES:
-
Exon skipping
- IR:
-
Intron retention
- RRM:
-
RNA recognition motif
- SR:
-
Serine/arginine-rich
- 3′SS:
-
Alternative 3′ splice site
- 5′SS:
-
Alternative 5′ splice site
References
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202–W208. https://doi.org/10.1093/nar/gkp335
Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18(9):1381–1392. https://doi.org/10.1101/gr.053678.106
Barta A, Kalyna M, Reddy AS (2010) Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22(9):2926–2929. https://doi.org/10.1105/tpc.110.078352
Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336. https://doi.org/10.1146/annurev.biochem.72.121801.161720
Brown JW, Smith P, Simpson CG (1996) Arabidopsis consensus intron sequences. Plant Mol Biol 32(3):531–535. https://doi.org/10.1007/BF00019105
Butt H, Piatek A, Li L, Reddy ASN, Mahfouz MM (2019) Multiplex CRISPR mutagenesis of the serine/arginine-rich (SR) gene family in rice. Genes (Basel) 10(8):596. https://doi.org/10.3390/genes10080596
Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5(3):250–257. https://doi.org/10.1016/s1369-5266(02)00255-8
Chen S, Li J, Liu Y, Li H (2019) Genome-wide analysis of serine/arginine-rich protein family in wheat and Brachypodium distachyon. Plants (Basel) 8(7):188. https://doi.org/10.3390/plants8070188
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Ding F, Cui P, Wang Z, Zhang S, Ali S, Xiong L (2014) Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genom 15:431. https://doi.org/10.1186/1471-2164-15-431
Duque P (2011) A role for SR proteins in plant stress responses. Plant Signal Behav 6(1):49–54. https://doi.org/10.4161/psb.6.1.14063
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47(D1):D427–D432. https://doi.org/10.1093/nar/gky995
Ferguson JN (2019) Climate change and abiotic stress mechanisms in plants. Emerg Top Life Sci 3(2):165–181. https://doi.org/10.1042/ETLS20180105
Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20(1):45–58. https://doi.org/10.1101/gr.093302.109
Gao H, Gordon-Kamm WJ, Lyznik LA (2004) ASF/SF2-like maize pre-mRNA splicing factors affect splice site utilization and their transcripts are alternatively spliced. Gene 339:25–37. https://doi.org/10.1016/j.gene.2004.06.047
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31(13):3784–3788. https://doi.org/10.1093/nar/gkg563
Graveley BR (2001) Alternative splicing: increasing diversity in the proteomic world. Trends Genet 17(2):100–107. https://doi.org/10.1016/s0168-9525(00)02176-4
Graveley BR, Hertel KJ, Maniatis T (1999) SR proteins are ‘locators’ of the RNA splicing machinery. Curr Biol 9(1):R6-7. https://doi.org/10.1016/s0960-9822(99)80032-3
Gu J, Xia Z, Luo Y, Jiang X, Qian B, Xie H, Zhu JK, Xiong L, Zhu J, Wang ZY (2018) Spliceosomal protein U1A is involved in alternative splicing and salt stress tolerance in Arabidopsis thaliana. Nucleic Acids Res 46(4):1777–1792. https://doi.org/10.1093/nar/gkx1229
Gu J, Ma S, Zhang Y, Wang D, Cao S, Wang ZY (2020) Genome-wide identification of cassava serine/arginine-rich proteins: insights into alternative splicing of pre-mRNAs and response to abiotic stress. Plant Cell Physiol 61(1):178–191. https://doi.org/10.1093/pcp/pcz190
Gupta S, Wang BB, Stryker GA, Zanetti ME, Lal SK (2005) Two novel arginine/serine (SR) proteins in maize are differentially spliced and utilize non-canonical splice sites. Biochim Biophys Acta 1728(3):105–114. https://doi.org/10.1016/j.bbaexp.2005.01.004
Haak DC, Fukao T, Grene R, Hua Z, Ivanov R, Perrella G, Li S (2017) Multilevel regulation of abiotic stress responses in plants. Front Plant Sci 8:1564. https://doi.org/10.3389/fpls.2017.01564
Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res 26(1):358–359. https://doi.org/10.1093/nar/26.1.358
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Huang R, Xiao D, Wang X, Zhan J, Wang A, He L (2022) Genome-wide identification, evolutionary and expression analyses of LEA gene family in peanut (Arachis hypogaea L.). BMC Plant Biol 22(1):155. https://doi.org/10.1186/s12870-022-03462-7
Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, Yan BY, Donohue JP, Shiue L, Hoon S, Brenner S, Ares M Jr, Yeo GW (2012) Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 1(2):167–178. https://doi.org/10.1016/j.celrep.2012.02.001
Isshiki M, Tsumoto A, Shimamoto K (2006) The serine/arginine-rich protein family in rice plays important roles in constitutive and alternative splicing of pre-mRNA. Plant Cell 18(1):146–158. https://doi.org/10.1105/tpc.105.037069
Jiang J, Liu X, Liu C, Liu G, Li S, Wang L (2017) Integrating omics and alternative splicing reveals insights into grape response to high temperature. Plant Physiol 173(2):1502–1518. https://doi.org/10.1104/pp.16.01305
Jiu S, Xu Y, Wang J, Wang L, Wang S, Ma C, Guan L, Abdullah M, Zhao M, Xu W, Ma W, Zhang C (2019) Genome-wide identification, characterization, and transcript analysis of the TCP transcription factors in Vitis vinifera. Front Genet 10:1276. https://doi.org/10.3389/fgene.2019.01276
Kalyna M, Barta A (2004) A plethora of plant serine/arginine-rich proteins: redundancy or evolution of novel gene functions? Biochem Soc Trans 32(Pt 4):561–564. https://doi.org/10.1042/BST0320561
Kalyna M, Lopato S, Voronin V, Barta A (2006) Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins. Nucleic Acids Res 34(16):4395–4405. https://doi.org/10.1093/nar/gkl570
Keller M, Hu Y, Mesihovic A, Fragkostefanakis S, Schleiff E, Simm S (2017) Alternative splicing in tomato pollen in response to heat stress. DNA Res 24(2):205–217. https://doi.org/10.1093/dnares/dsw051
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Laloum T, Martin G, Duque P (2018) Alternative splicing control of abiotic stress responses. Trends Plant Sci 23(2):140–150. https://doi.org/10.1016/j.tplants.2017.09.019
Lee KC, Jang YH, Kim SK, Park HY, Thu MP, Lee JH, Kim JK (2017) RRM domain of Arabidopsis splicing factor SF1 is important for pre-mRNA splicing of a specific set of genes. Plant Cell Rep 36(7):1083–1095. https://doi.org/10.1007/s00299-017-2140-1
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (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(1):325–327. https://doi.org/10.1093/nar/30.1.325
Ling Y, Alshareef S, Butt H, Lozano-Juste J, Li L, Galal AA, Moustafa A, Momin AA, Tashkandi M, Richardson DN, Fujii H, Arold S, Rodriguez PL, Duque P, Mahfouz MM (2017) Pre-mRNA splicing repression triggers abiotic stress signaling in plants. Plant J 89(2):291–309. https://doi.org/10.1111/tpj.13383
Ling Y, Serrano N, Gao G, Atia M, Mokhtar M, Woo YH, Bazin J, Veluchamy A, Benhamed M, Crespi M, Gehring C, Reddy ASN, Mahfouz MM (2018) Thermopriming triggers splicing memory in Arabidopsis. J Exp Bot 69(10):2659–2675. https://doi.org/10.1093/jxb/ery062
Ling Y, Mahfouz MM, Zhou S (2021) Pre-mRNA alternative splicing as a modulator for heat stress response in plants. Trends Plant Sci 26(11):1153–1170. https://doi.org/10.1016/j.tplants.2021.07.008
Liu J, Sun N, Liu M, Liu J, Du B, Wang X, Qi X (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol 162(1):512–521. https://doi.org/10.1104/pp.112.205864
Lopato S, Waigmann E, Barta A (1996) Characterization of a novel arginine/serine-rich splicing factor in Arabidopsis. Plant Cell 8(12):2255–2264. https://doi.org/10.1105/tpc.8.12.2255
Lopez AJ (1998) Alternative splicing of pre-mRNA: developmental consequences and mechanisms of regulation. Annu Rev Genet 32:279–305. https://doi.org/10.1146/annurev.genet.32.1.279
Ma X, He F (2003) Advances in the study of SR protein family. Genom Proteom Bioinform 1(1):2–8. https://doi.org/10.1016/s1672-0229(03)01002-7
Palusa SG, Ali GS, Reddy AS (2007) Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J 49(6):1091–1107. https://doi.org/10.1111/j.1365-313X.2006.03020.x
Reddy AS, Shad Ali G (2011) Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip Rev RNA 2(6):875–889. https://doi.org/10.1002/wrna.98
Rosenkranz RRE, Bachiri S, Vraggalas S, Keller M, Simm S, Schleiff E, Fragkostefanakis S (2021) Identification and regulation of tomato serine/arginine-rich proteins under high temperatures. Front Plant Sci 12:645689. https://doi.org/10.3389/fpls.2021.645689
Roth MB, Zahler AM, Stolk JA (1991) A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J Cell Biol 115(3):587–596. https://doi.org/10.1083/jcb.115.3.587
Schoning JC, Streitner C, Meyer IM, Gao Y, Staiger D (2008) Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res 36(22):6977–6987. https://doi.org/10.1093/nar/gkn847
Subramanian B, Gao S, Lercher MJ, Hu S, Chen WH (2019) Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Res 47(W1):W270–W275. https://doi.org/10.1093/nar/gkz357
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang BB, Brendel V (2006) Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci USA 103(18):7175–7180. https://doi.org/10.1073/pnas.0602039103
Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456(7221):470–476. https://doi.org/10.1038/nature07509
Wang S, Nie S, Zhu F (2016) Chemical constituents and health effects of sweet potato. Food Res Int 89(Pt 1):90–116. https://doi.org/10.1016/j.foodres.2016.08.032
Wang TY, Liu Q, Ren Y, Alam SK, Wang L, Zhu Z, Hoeppner LH, Dehm SM, Cao Q, Yang R (2021) A pan-cancer transcriptome analysis of exitron splicing identifies novel cancer driver genes and neoepitopes. Mol Cell 81(10):2246-2260.e2212. https://doi.org/10.1016/j.molcel.2021.03.028
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552. https://doi.org/10.1385/1-59259-584-7:531
Will CL, Luhrmann R (2011) Spliceosome structure and function. Cold Spring Harb Perspect Biol 3(7):a003707. https://doi.org/10.1101/cshperspect.a003707
Wu Z, Liang J, Wang C, Ding L, Zhao X, Cao X, Xu S, Teng N, Yi M (2019) Alternative splicing provides a mechanism to regulate LlHSFA3 function in response to heat stress in lily. Plant Physiol 181(4):1651–1667. https://doi.org/10.1104/pp.19.00839
Yu H, Tian C, Yu Y, Jiao Y (2016) Transcriptome survey of the contribution of alternative splicing to proteome diversity in Arabidopsis thaliana. Mol Plant 9(5):749–752. https://doi.org/10.1016/j.molp.2015.12.018
Yu Y, Pan Z, Wang X, Bian X, Wang W, Liang Q, Kou M, Ji H, Li Y, Ma D, Li Z, Sun J (2021) Targeting of SPCSV-RNase3 via CRISPR-Cas13 confers resistance against sweet potato virus disease. Mol Plant Pathol 23:104–117. https://doi.org/10.1111/mpp.13146
Zhang P, Deng H, Xiao F-M, Liu Y-S (2013) Alterations of alternative splicing patterns of Ser/Arg-rich (SR) genes in response to hormones and stresses treatments in different ecotypes of rice (Oryza sativa). J Integr Agric 12(5):737–748
Zhang XN, Mo C, Garrett WM, Cooper B (2014) Phosphothreonine 218 is required for the function of SR45.1 in regulating flower petal development in Arabidopsis. Plant Signal Behav 9(7):e29134. https://doi.org/10.4161/psb.29134
Zhu W, Schlueter SD, Brendel V (2003) Refined annotation of the Arabidopsis genome by complete expressed sequence tag mapping. Plant Physiol 132(2):469–484. https://doi.org/10.1104/pp.102.018101
Acknowledgements
This study was funded by the Basic and Applied Basic Research Foundation of GuangDong Province, China (Grant No. 2021A1515012391), GDOU Innovation & University Improvement Program (Grant No. 230419099) and GDOU Talent Introduction Project (Grant No. R19015).
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Supplementary file4 (JPG 1475 KB)—Figure S1. The RT-PCR results of 31 sweet potato SR-similar genes.
425_2022_3965_MOESM5_ESM.jpg
Supplementary file 5 (JPG 3081 KB)—Figure S2. The qRT-PCR results of 31 sweet potato SR-similar genes. Three biological replicates were set up and the relative gene expression levels were calculated by 2−ΔΔCt method. The error bars indicate ± SE, lowercase letters indicate α = 0.05 significant level. ARF was selected as the reference gene.
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Chen, S., Mo, Y., Zhang, Y. et al. Insights into sweet potato SR proteins: from evolution to species-specific expression and alternative splicing. Planta 256, 72 (2022). https://doi.org/10.1007/s00425-022-03965-5
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DOI: https://doi.org/10.1007/s00425-022-03965-5