Skip to main content

Advertisement

SpringerLink
Log in

Alternative Splicing for Improving Abiotic Stress Tolerance and Agronomic Traits in Crop Plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Most eukaryotic genes undergo various post-transcriptional processing events before being translated into proteins. Alternative splicing (AS) is one such event and is an essential mechanism in post-transcriptional gene regulation that allows multiple mRNA variants to be expressed from a single pre-mRNA, thereby expending the functional capacity of a gene as well as the organismal complexity. With the advancement of next-generation sequencing technologies, extensive transcriptomic resources in plant species have determined crucial roles of AS in the regulation of developmental processes and adaption to environmental stresses. We review here recent studies of AS events and splicing factors that specifically affect abiotic-stress tolerance in crop plants, including other agricultural traits. Understanding how alternative splicing modulates plant development and abiotic-stress responses may provide new insights for improving the environmental fitness and productivity of crop plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Siden-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, Woodage T, Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287(5461):2185–2195

    Article  PubMed  Google Scholar 

  • Amirbakhtiar N, Ismaili A, Ghaffari MR, Nazarian Firouzabadi F, Shobbar ZS (2019) Transcriptome response of roots to salt stress in a salinity-tolerant bread wheat cultivar. PLoS ONE 14(3):e0213305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arabidopsis Genome I (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815

    Article  Google Scholar 

  • Ast G (2004) How did alternative splicing evolve? Nat Rev Genet 5(10):773–782

    Article  CAS  PubMed  Google Scholar 

  • Baralle FE, Giudice J (2017) Alternative splicing as a regulator of development and tissue identity. Nat Rev Mol Cell Biol 18(7):437–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ (2010) Deciphering the splicing code. Nature 465(7294):53–59

    Article  CAS  PubMed  Google Scholar 

  • Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Colak R, Kim T, Misquitta-Ali CM, Wilson MD, Kim PM, Odom DT, Frey BJ, Blencowe BJ (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science 338(6114):1587–1593

    Article  CAS  PubMed  Google Scholar 

  • Bazin J, Mariappan K, Jiang Y, Blein T, Voelz R, Crespi M, Hirt H (2020) Role of MPK4 in pathogen-associated molecular pattern-triggered alternative splicing in Arabidopsis. PLoS Pathog 16(4):e1008401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336

    Article  CAS  PubMed  Google Scholar 

  • Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126(1):37–47

    Article  CAS  PubMed  Google Scholar 

  • Blencowe BJ, Bowman JA, McCracken S, Rosonina E (1999) SR-related proteins and the processing of messenger RNA precursors. Biochem Cell Biol 77(4):277–291

    Article  CAS  PubMed  Google Scholar 

  • Boscari A, Del Giudice J, Ferrarini A, Venturini L, Zaffini AL, Delledonne M, Puppo A (2013) Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol 161(1):425–439

    Article  CAS  PubMed  Google Scholar 

  • Buratti E, Stuani C, De Prato G, Baralle FE (2007) SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res 35(13):4359–4368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bush SJ, Chen L, Tovar-Corona JM, Urrutia AO (2017) Alternative splicing and the evolution of phenotypic novelty. Philos Trans R Soc Lond B Biol Sci 372(1713)

  • Caputi M, Zahler AM (2002) SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J 21(4):845–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 31(13):3568–3571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chasin LA (2007) Searching for splicing motifs. Adv Exp Med Biol 623:85–106

    Article  PubMed  Google Scholar 

  • Chen H, Chen X, Chen D, Li J, Zhang Y, Wang A (2015) A comparison of the low temperature transcriptomes of two tomato genotypes that differ in freezing tolerance: Solanum lycopersicum and Solanum habrochaites. BMC Plant Biol 15:132

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen L, Li W, Li Y, Feng X, Du K, Wang G, Zhao L (2019) Identified trans-splicing of YELLOW-FRUITED TOMATO 2 encoding the PHYTOENE SYNTHASE 1 protein alters fruit color by map-based cloning, functional complementation and RACE. Plant Mol Biol, pp 1–12

  • Chiou NT, Shankarling G, Lynch KW (2013) hnRNP L and hnRNP A1 induce extended U1 snRNA interactions with an exon to repress spliceosome assembly. Mol Cell 49(5):972–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark S, Yu F, Gu L, Min XJ (2019) Expanding alternative splicing identification by integrating multiple sources of transcription data in tomato. Front Plant Sci 10:689

    Article  PubMed  PubMed Central  Google Scholar 

  • Crawford JB, Patton JG (2006) Activation of alpha-tropomyosin exon 2 is regulated by the SR protein 9G8 and heterogeneous nuclear ribonucleoproteins H and F. Mol Cell Biol 26(23):8791–8802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das N, Bhattacharya S, Bhattacharyya S, Maiti MK (2017) Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol 94(1–2):167–183

    Article  CAS  PubMed  Google Scholar 

  • Ding N, Cui H, Miao Y, Tang J, Cao Q, Luo Y (2019) Single-molecule real-time sequencing identifies massive full-length cDNAs and alternative-splicing events that facilitate comparative and functional genomics study in the hexaploid crop sweet potato. PeerJ 7:e7933

    Article  PubMed  PubMed Central  Google Scholar 

  • Domsic JK, Wang Y, Mayeda A, Krainer AR, Stoltzfus CM (2003) Human immunodeficiency virus type 1 hnRNP A/B-dependent exonic splicing silencer ESSV antagonizes binding of U2AF65 to viral polypyrimidine tracts. Mol Cell Biol 23(23):8762–8772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong C, He F, Berkowitz O, Liu J, Cao P, Tang M, Shi H, Wang W, Li Q, Shen Z, Whelan J, Zheng L (2018) Alternative splicing plays a critical role in maintaining mineral nutrient homeostasis in rice (Oryza sativa). Plant Cell 30(10):2267–2285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du J, Li Y, Sun X, Yu L, Jiang H, Cao Q, Shang J, Sun M, Liu Y, Shu K, Liu J, Yong T, Liu W, Yang F, Wang X, Liu C, Yang W (2018) Characterization of a splice variant of soybean ERECTA devoid of an intracellular kinase domain in response to shade stress. J Genet 97(5):1353–1361

    Article  CAS  PubMed  Google Scholar 

  • Egawa C, Kobayashi F, Ishibashi M, Nakamura T, Nakamura C, Takumi S (2006) Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Syst 81(2):77–91

    Article  CAS  PubMed  Google Scholar 

  • Expert-Bezancon A, Sureau A, Durosay P, Salesse R, Groeneveld H, Lecaer JP, Marie J (2004) hnRNP A1 and the SR proteins ASF/SF2 and SC35 have antagonistic functions in splicing of beta-tropomyosin exon 6B. J Biol Chem 279(37):38249–38259

    Article  CAS  PubMed  Google Scholar 

  • Favero Peixoto-Junior R, Mara de Andrade L, Dos Santos Brito M, Macedo Nobile P, Palma Boer Martins A, Domingues Carlin S, Vasconcelos Ribeiro R, de Souza Goldman MH, de Oliveira JFNC, de Oliveira Figueria AV, Creste S (2018) Overexpression of ScMYBAS1 alternative splicing transcripts differentially impacts biomass accumulation and drought tolerance in rice transgenic plants. PLoS ONE 13(12):e0207534

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu L, Shen Q, Kuang L, Wu D, Zhang G (2019) Transcriptomic and alternative splicing analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Environ Exp Bot 166:103810

    Article  CAS  Google Scholar 

  • Garneau D, Revil T, Fisette JF, Chabot B (2005) Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 280(24):22641–22650

    Article  CAS  PubMed  Google Scholar 

  • Geng X, Zang X, Li H, Liu Z, Zhao A, Liu J, Peng H, Yao Y, Hu Z, Ni Z, Sun Q, Xin M (2018) Unconventional splicing of wheat TabZIP60 confers heat tolerance in transgenic Arabidopsis. Plant Sci 274:252–260

    Article  CAS  PubMed  Google Scholar 

  • Graveley BR (2000) Sorting out the complexity of SR protein functions. RNA 6(9):1197–1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory TR (2005) Synergy between sequence and size in large-scale genomics. Nat Rev Genet 6(9):699–708

    Article  CAS  PubMed  Google Scholar 

  • Han N, Ji XL, Du YP, He X, Zhao XJ, Zhai H (2017) Identification of a novel alternative splicing variant of VvPMA1 in grape root under salinity. Front Plant Sci 8:605

    Article  PubMed  PubMed Central  Google Scholar 

  • Heiner M, Hui J, Schreiner S, Hung LH, Bindereif A (2010) HnRNP L-mediated regulation of mammalian alternative splicing by interference with splice site recognition. RNA Biol 7(1):56–64

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Mesihovic A, Jiménez-Gómez JM, Röth S, Gebhardt P, Bublak D, Bovy A, Scharf KD, Schleiff E, Fragkostefanakis S (2020) Natural variation in HsfA2 pre-mRNA splicing is associated with changes in thermotolerance during tomato domestication. New Phytol 225(3):1297–1310

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537(7622):629–633

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim EC, Schaal TD, Hertel KJ, Reed R, Maniatis T (2005) Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers. Proc Natl Acad Sci USA 102(14):5002–5007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacquenet S, Mereau A, Bilodeau PS, Damier L, Stoltzfus CM, Branlant C (2001) A second exon splicing silencer within human immunodeficiency virus type 1 tat exon 2 represses splicing of Tat mRNA and binds protein hnRNP H. J Biol Chem 276(44):40464–40475

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Ma X, Zhao S, Tang Y, Liu F, Gu P, Fu Y, Zhu Z, Cai H, Sun C, Tan L (2019) The APETALA2-like transcription factor SUPERNUMERARY BRACT controls rice seed shattering and seed size. Plant Cell 31(1):17–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Meyerowitz EM (2010) Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol Syst Biol 6:419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12(1):5–14

    Article  CAS  PubMed  Google Scholar 

  • Lee SS, Jung WY, Park HJ, Lee A, Kwon SY, Kim HS, Cho HS (2018) Genome-wide analysis of alternative splicing in an inbred cabbage (Brassica oleracea L.) line 'HO' in response to heat stress. Curr Genomics 19(1):12–20

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Guo Y, Cui W, Xu A, Tian Z (2014) Response of maize serine/arginine-rich protein gene family in seedlings to drought stress. Hereditas 36(7):697–706

    PubMed  Google Scholar 

  • Li R, Wang W, Li F, Wang Q, Wang S, Xu Y, Chen F (2017a) Response of alternative splice isoforms of OsRad9 gene from Oryza sativa to environmental stress. Z Naturforsch C J Biosci 72(7–8):325–334

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Dai C, Hu C, Liu Z, Kang C (2017b) Global identification of alternative splicing via comparative analysis of SMRT- and illumina-based RNA-seq in strawberry. Plant J 90(1):164–176

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Wu X, Yao X, Yu R, Larkin PJ, Liu CM (2018a) Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains. Proc Natl Acad Sci USA 115(44):11327–11332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Qin J, Tian X, Xu S, Wang Y, Li H, Wang X, Peng H, Yao Y, Hu Z (2018b) Global profiling of alternative splicing landscape responsive to drought, heat and their combination in wheat (Triticum aestivum L.). Plant Biotechnol J 16(3):714–726

    Article  CAS  PubMed  Google Scholar 

  • Loraine AE, McCormick S, Estrada A, Patel K, Qin P (2013) RNA-seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162(2):1092–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20(9):1238–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Zhao P, Zhang A, Ma L, Xu S, Wang X (2019) Alternative splicing diversifies the heat response and evolutionary strategy of conserved Heat Shock Protein 90 in bread wheat (Triticum aestivum L.). Res Square. https://doi.org/10.21203/rs.3.rs-63027/v1

  • Luo X, Xu L, Liang D, Wang Y, Zhang W, Zhu X, Zhu Y, Jiang H, Tang M, Liu L (2017) Comparative transcriptomics uncovers alternative splicing and molecular marker development in radish (Raphanus sativus L.). BMC Genomics 18(1):505

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo M, Ding J, Li Y, Tang H, Qi P, Ma J, Wang J, Chen G, Pu Z, Li W (2019) A single-base change at a splice site in Wx-A1 caused incorrect RNA splicing and gene inactivation in a wheat EMS mutant line. Theor Appl Genet 132(7):2097–2109

    Article  CAS  PubMed  Google Scholar 

  • Mandadi KK, Scholthof KB (2015) Genome-wide analysis of alternative splicing landscapes modulated during plant-virus interactions in Brachypodium distachyon. Plant Cell 27(1):71–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22(6):1184–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marulanda A, Azcon R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232(2):533–543

    Article  CAS  PubMed  Google Scholar 

  • Mathew IE, Das S, Mahto A, Agarwal P (2016) Three rice NAC transcription factors heteromerize and are associated with seed size. Front Plant Sci 7:1638

    Article  PubMed  PubMed Central  Google Scholar 

  • Matlin AJ, Clark F, Smith CW (2005) Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 6(5):386–398

    Article  CAS  PubMed  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics 283(2):185–196

    Article  CAS  PubMed  Google Scholar 

  • Mauger DM, Lin C, Garcia-Blanco MA (2008) hnRNP H and hnRNP F complex with Fox2 to silence fibroblast growth factor receptor 2 exon IIIc. Mol Cell Biol 28(17):5403–5419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Mei W, Liu S, Schnable JC, Yeh CT, Springer NM, Schnable PS, Barbazuk WB (2017) A comprehensive analysis of alternative splicing in paleopolyploid maize. Front Plant Sci 8:694

    Article  PubMed  PubMed Central  Google Scholar 

  • Mills JD, Janitz M (2012) Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol Aging 33(5):1012.e11–1012.e24

    Article  CAS  Google Scholar 

  • Min XJ, Powell B, Braessler J, Meinken J, Yu F, Sablok G (2015) Genome-wide cataloging and analysis of alternatively spliced genes in cereal crops. BMC Genomics 16:721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mirdar Mansuri R, Shobbar ZS, Babaeian Jelodar N, Ghaffari MR, Nematzadeh GA, Asari S (2019) Dissecting molecular mechanisms underlying salt tolerance in rice: a comparative transcriptional profiling of the contrasting genotypes. Rice 12(1):13

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40(12):1413–1415

    Article  CAS  PubMed  Google Scholar 

  • Park E, Iaccarino C, Lee J, Kwon I, Baik SM, Kim M, Seong JY, Son GH, Borrelli E, Kim K (2011) Regulatory roles of heterogeneous nuclear ribonucleoprotein M and Nova-1 protein in alternative splicing of dopamine D2 receptor pre-mRNA. J Biol Chem 286(28):25301–25308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng P, Gao Y, Li Z, Yu Y, Qin H, Guo Y, Huang R, Wang J (2019) Proteomic analysis of a rice mutant sd58 possessing a novel d1 allele of heterotrimeric G protein alpha subunit (RGA1) in salt stress with a focus on ROS scavenging. Int J Mol Sci 20(1):167

    Article  PubMed Central  CAS  Google Scholar 

  • Pistoni M, Ghigna C, Gabellini D (2010) Alternative splicing and muscular dystrophy. RNA Biol 7(4):441–452

    Article  CAS  PubMed  Google Scholar 

  • Qiao D, Yang C, Chen J, Guo Y, Li Y, Niu S, Cao K, Chen Z (2019) Comprehensive identification of the full-length transcripts and alternative splicing related to the secondary metabolism pathways in the tea plant (Camellia sinensis). Sci Rep 9(1):2709

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50(1):54–69

    Article  CAS  PubMed  Google Scholar 

  • Reddy AS, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25(10):3657–3683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed R (1996) Initial splice-site recognition and pairing during pre-mRNA splicing. Curr Opin Genet Dev 6(2):215–220

    Article  CAS  PubMed  Google Scholar 

  • Rigo R, Bazin JRM, Crespi M, Charon CL (2019) Alternative splicing in the regulation of plant-microbe interactions. Plant Cell Physiol 60(9):1906–1916

    Article  CAS  PubMed  Google Scholar 

  • Roman A, Andreu V, Hernandez ML, Lagunas B, Picorel R, Martinez-Rivas JM, Alfonso M (2012) Contribution of the different omega-3 fatty acid desaturase genes to the cold response in soybean. J Exp Bot 63(13):4973–4982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sablok G, Powell B, Braessler J, Yu F, Min XJ (2017) Comparative landscape of alternative splicing in fruit plants. Curr Plant Biol 9:29–36

    Article  Google Scholar 

  • Sharma A, Shankhdhar D, Shankhdhar S (2013) Enhancing grain iron content of rice by the application of plant growth promoting rhizobacteria. Plant Soil Environ 59(2):89–94

    Article  CAS  Google Scholar 

  • Shavrukov Y, Zhumalin A, Serikbay D, Botayeva M, Otemisova A, Absattarova A, Sereda G, Sereda S, Shvidchenko V, Turbekova A, Jatayev S, Lopato S, Soole K, Langridge P (2016) Expression level of the DREB2-type gene, identified with amplifluor SNP markers, correlates with performance, and tolerance to dehydration in bread wheat cultivars from Northern Kazakhstan. Front Plant Sci 7:1736

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Zhou Z, Wang Z, Li W, Fang C, Wu M, Ma Y, Liu T, Kong LA, Peng DL, Tian Z (2014) Global dissection of alternative splicing in paleopolyploid soybean. Plant Cell 26(3):996–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmonds J, Scott P, Brinton J, Mestre TC, Bush M, Del Blanco A, Dubcovsky J, Uauy C (2016) A splice acceptor site mutation in TaGW2-A1 increases thousand grain weight in tetraploid and hexaploid wheat through wider and longer grains. Theor Appl Genet 129(6):1099–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solis AS, Peng R, Crawford JB, Phillips JA 3rd, Patton JG (2008) Growth hormone deficiency and splicing fidelity: two serine/arginine-rich proteins, ASF/SF2 and SC35, act antagonistically. J Biol Chem 283(35):23619–23626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song H, Dong X, Yi H, Ahn JY, Yun K, Song M, Han CT, Hur Y (2018) Genome-wide identification and characterization of warming-related genes in Brassica rapa ssp. pekinensis. Int J Mol Sci 19(6):1727

    Article  PubMed Central  CAS  Google Scholar 

  • Staiger D, Brown JW (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25(10):3640–3656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su Z, Hao C, Wang L, Dong Y, Zhang X (2011) Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122(1):211–223

    Article  CAS  PubMed  Google Scholar 

  • Suarez C, Cardinale M, Ratering S, Steffens D, Jung S, Montoya AMZ, Geissler-Plaum R, Schnell S (2015) Plant growth-promoting effects of Hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl Soil Ecol 95:23–30

    Article  Google Scholar 

  • Syed NH, Prince SJ, Mutava RN, Patil G, Li S, Chen W, Babu V, Joshi T, Khan S, Nguyen HT (2015) Core clock, SUB1, and ABAR genes mediate flooding and drought responses via alternative splicing in soybean. J Exp Bot 66(22):7129–7149

    Article  CAS  PubMed  Google Scholar 

  • Talukdar I, Sen S, Urbano R, Thompson J, Yates JR 3rd, Webster NJ (2011) hnRNP A1 and hnRNP F modulate the alternative splicing of exon 11 of the insulin receptor gene. PLoS ONE 6(11):e27869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tazi J, Bakkour N, Stamm S (2009) Alternative splicing and disease. Biochim Biophys Acta 1792(1):14–26

    Article  CAS  PubMed  Google Scholar 

  • ten Dam GB, Zilch CF, Wallace D, Wieringa B, Beverley PC, Poels LG, Screaton GR (2000) Regulation of alternative splicing of CD45 by antagonistic effects of SR protein splicing factors. J Immunol 164(10):5287–5295

    Article  PubMed  Google Scholar 

  • Terashima A, Takumi S (2009) Allopolyploidization reduces alternative splicing efficiency for transcripts of the wheat DREB2 homolog, WDREB2. Genome 52(1):100–105

    Article  CAS  PubMed  Google Scholar 

  • Thatcher SR, Zhou W, Leonard A, Wang BB, Beatty M, Zastrow-Hayes G, Zhao X, Baumgarten A, Li B (2014) Genome-wide analysis of alternative splicing in Zea mays: landscape and genetic regulation. Plant Cell 26(9):3472–3487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thatcher SR, Danilevskaya ON, Meng X, Beatty M, Zastrow-Hayes G, Harris C, Van Allen B, Habben J, Li B (2016) Genome-wide analysis of alternative splicing during development and drought stress in maize. Plant Physiol 170(1):586–599

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Zhao X, Liu H, Ku L, Wang S, Han Z, Wu L, Shi Y, Song X, Chen Y (2019) Alternative splicing of ZmCCA1 mediates drought response in tropical maize. PLoS ONE 14(1):e0211623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twyffels L, Gueydan C, Kruys V (2011) Shuttling SR proteins: more than splicing factors. FEBS J 278(18):3246–3255

    Article  CAS  PubMed  Google Scholar 

  • Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, Gabor Miklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C, Yao A, Ye J, Zhan M, Zhang W, Zhang H, Zhao Q, Zheng L, Zhong F, Zhong W, Zhu S, Zhao S, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An H, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigo R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi H, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Mays A, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu X, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen M, Wu D, Wu M, Xia A, Zandieh A, Zhu X (2001) The sequence of the human genome. Science 291(5507):1304–1351

    Article  CAS  PubMed  Google Scholar 

  • Vitulo N, Forcato C, Carpinelli EC, Telatin A, Campagna D, D'Angelo M, Zimbello R, Corso M, Vannozzi A, Bonghi C, Lucchin M, Valle G (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14:99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wahl MC, Will CL, Luhrmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136(4):701–718

    Article  CAS  PubMed  Google Scholar 

  • Wai CM, Powell B, Ming R, Min XJ (2016) Analysis of alternative splicing landscape in pineapple (Ananas comosus). Trop Plant Biol 9(3):150–160

    Article  CAS  Google Scholar 

  • Wang Z, Rolish ME, Yeo G, Tung V, Mawson M, Burge CB (2004) Systematic identification and analysis of exonic splicing silencers. Cell 119(6):831–845

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Dimova N, Cambi F (2007) PLP/DM20 ratio is regulated by hnRNPH and F and a novel G-rich enhancer in oligodendrocytes. Nucleic Acids Res 35(12):4164–4178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Yuan F, Hao H, Zhang Y, Zhao H, Guo A, Hu J, Zhou X, Xie CG (2013) BolOST1, an ortholog of Open Stomata 1 with alternative splicing products in Brassica oleracea, positively modulates drought responses in plants. Biochem Biophys Res Commun 442(3–4):214–220

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Liu J, Huang BO, Xu YM, Li J, Huang LF, Lin J, Zhang J, Min QH, Yang WM, Wang XZ (2015) Mechanism of alternative splicing and its regulation. Biomed Rep 3(2):152–158

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Wang P, Liang F, Ye Z, Li J, Shen C, Pei L, Wang F, Hu J, Tu L, Lindsey K, He D, Zhang X (2018) A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation. New Phytol 217(1):163–178

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Tang S, Zhan Q, Hou Q, Zhao Y, Zhao Q, Feng Q, Zhou C, Lyu D, Cui L, Li Y, Miao J, Zhu C, Lu Y, Wang Y, Wang Z, Zhu J, Shangguan Y, Gong J, Yang S, Wang W, Zhang J, Xie H, Huang X, Han B (2019a) Dissecting a heterotic gene through GradedPool-Seq mapping informs a rice-improvement strategy. Nat Commun 10(1):2982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang X, Chen S, Shi X, Liu D, Zhao P, Lu Y, Cheng Y, Liu Z, Nie X, Song W (2019b) Hybrid sequencing reveals insight into heat sensing and signaling of bread wheat. Plant J 98(6):1015–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Zhang H, Gong W (2019c) Genome-wide identification and comparative analysis of alternative splicing across four legume species. Planta 249(4):1133–1142

    Article  CAS  PubMed  Google Scholar 

  • Wei H, Lou Q, Xu K, Yan M, Xia H, Ma X, Yu X, Luo L (2017) Alternative splicing complexity contributes to genetic improvement of drought resistance in the rice maintainer HuHan2B. Sci Rep 7(1):11686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu W, Li R, Zhang N, Ma F, Jiao Y, Wang Z (2014) Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress. Plant Mol Biol 86(4–5):527–541

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Zeng A, Song L, Li J, Yan J (2019) Comparative transcriptomics analysis uncovers alternative splicing events and molecular markers in cabbage (Brassica oleracea L.). Planta 249(5):1599–1615

    Article  CAS  PubMed  Google Scholar 

  • Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37(3):326–339

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Pu Y, Yin X, Du J, Zhou Z, Yang D, Sun X, Sun H, Yang Y (2019) A splice variant of BrrWSD1 in Turnip (Brassica rapa var. rapa) and its possible role in wax ester synthesis under drought stress. J Agric Food Chem 67(40):11077–11088

    Article  CAS  PubMed  Google Scholar 

  • Yoon EK, Krishnamurthy P, Kim JA, Jeong M-J, Lee SI (2018) Genome-wide characterization of Brassica rapa genes encoding serine/arginine-rich proteins: expression and alternative splicing events by abiotic stresses. J Plant Biol 61(4):198–209

    Article  CAS  Google Scholar 

  • Yu J, Miao J, Zhang Z, Xiong H, Zhu X, Sun X, Pan Y, Liang Y, Zhang Q, Abdul Rehman RM, Li J, Zhang H, Li Z (2018) Alternative splicing of OsLG3b controls grain length and yield in japonica rice. Plant Biotechnol J 16(9):1667–1678

    Article  CAS  PubMed Central  Google Scholar 

  • Yuan FJ, Zhu DH, Tan YY, Dong DK, Fu XJ, Zhu SL, Li BQ, Shu QY (2012) Identification and characterization of the soybean IPK1 ortholog of a low phytic acid mutant reveals an exon-excluding splice-site mutation. Theor Appl Genet 125(7):1413–1423

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Xiao B (2018) Comparative alternative splicing analysis of two contrasting rice cultivars under drought stress and association of differential splicing genes with drought response QTLs. Euphytica 214(4):73

    Article  CAS  Google Scholar 

  • Zhang G, Guo G, Hu X, Zhang Y, Li Q, Li R, Zhuang R, Lu Z, He Z, Fang X (2010) Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res 20(5):646–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang P, Heng D, 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

    Article  Google Scholar 

  • Zhang Q, Zhang X, Wang S, Tan C, Zhou G, Li C (2016) Involvement of alternative splicing in barley seed germination. PLoS ONE 11(3):e0152824

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Yan L, Zeng J, Zhou H, Liu H, Yu G, Yao W, Chen K, Ye Z, Xu H (2019) Pan-cancer analysis of clinical relevance of alternative splicing events in 31 human cancers. Oncogene 38(40):6678–6695

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Hu F, Zhang X, Wei Q, Dong J, Bo C, Cheng B, Ma Q (2019) Comparative transcriptome analysis reveals important roles of nonadditive genes in maize hybrid An'nong 591 under heat stress. BMC Plant Biol 19(1):273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou Z, Licklider LJ, Gygi SP, Reed R (2002) Comprehensive proteomic analysis of the human spliceosome. Nature 419(6903):182–185

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Mayeda A, Krainer AR (2001) Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol Cell 8(6):1351–1361

    Article  CAS  PubMed  Google Scholar 

  • Zhu G, Li W, Zhang F, Guo W (2018) RNA-seq analysis reveals alternative splicing under salt stress in cotton, Gossypium davidsonii. BMC Genomics 19(1):73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by a grant from Duksung Women’s University (3000003093 to T.-H. Kim).

Author information

Authors and Affiliations

  1. Department of Biotechnology, Program of Bio-Health Convergence, Duksung Women’s University, Seoul, 01369, Korea

    Seojung Kim & Tae-Houn Kim

Authors
  1. Seojung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tae-Houn Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tae-Houn Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, S., Kim, TH. Alternative Splicing for Improving Abiotic Stress Tolerance and Agronomic Traits in Crop Plants. J. Plant Biol. 63, 409–420 (2020). https://doi.org/10.1007/s12374-020-09282-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09282-2

Keywords

Search

Navigation