Biopolym. Cell. 2023; 39(2):110-130.
http://dx.doi.org/10.7124/bc.000A8E
Геноміка, транскриптоміка та протеоміка
Передбачення та аналіз стрес-індукованих транскрипційних факторів ICE у Deschampsia antarctica
1Бублик О. М., 1Андрєєв І. О., 1Кунах В. А.
  1. Інститут молекулярної біології і генетики НАН України
    Вул. Академіка Заболотного, 150, Київ, Україна, 03143

Abstract

Мета. Дослідження молекулярно-генетичних аспектів стресостійкості рослини-екстремофіла D. antarctica на прикладі аналізу транскрипційних факторів ICE, залучених до відповіді на холодовий стрес, регуляції розвитку продихів і часу цвітіння. Методи. Гени DaICE збирали із послідовностей, гомологічних до генів-ортологів, з бази даних SRA. Передбачені гени та білки аналізували біоінформатичними методами. Генну експресію аналізували з використанням даних секвенування РНК. Результати. Знайдено два варіанти гена DaICE1: типовий, який кодує повнорозмірний білок, та варіант із великою делецією, що призвела до втрати N-кінця та частини bHLH-домена у білкового продукта. Для гена DaICE2 знайдено два близькі варіанти з чотирма однонуклеотидними поліморфізмами, три з яких є синонімічними, в кодувальній ділянці та більш відмінними промоторними послідовностями. Досліджено організацію промоторів та інтрон-екзонну структуру генів. Для передбачених ТФ визначено фізико-хімічні властивості, показано локалізацію в ядрі, можливість посттрансляційних модифікацій, проведено філогенетичний аналіз, пошук консервативних мотивів, передбачено тривимірну структуру. Виявлено експресію генів у більшості або всіх тканинах та показано підвищену експресію варіантів DaICE1 в рослинах з природних умов, порівняно з лабораторними. Висновки. DaICE1 та DaICE2 є кандидатами на роль регуляторів експресії генів CBF під час холодового стресу у D. antarctica.
Keywords: антарктичні рослини, транскрипційні фактори, передбачення in silico, абіотичний стрес, стійкість
Повний текст: (PDF, англійською)

References

[1] Parnikoza I, Kozeretska I, Kunakh V. Vascular Plants of the Maritime Antarctic: Origin and Adaptation. Am J Plant Sci. 2011; 2(3):381-95.
[2] Byun MY, Lee J, Cui LH, Kang Y, Oh TK, Park H, Lee H, Kim WT. Constitutive expression of DaCBF7, an Antarctic vascular plant Deschampsia antarctica CBF homolog, resulted in improved cold tolerance in transgenic rice plants. Plant Sci. 2015; 236:61-74.
[3] Byun MY, Cui LH, Lee J, Park H, Lee A, Kim WT, Lee H. Identification of Rice Genes Associated With Enhanced Cold Tolerance by Comparative Transcriptome Analysis With Two Transgenic Rice Plants Overexpressing DaCBF4 or DaCBF7, Isolated From Antarctic Flowering Plant Deschampsia antarctica. Front Plant Sci. 2018; 9:601.
[4] Byun MY, Cui LH, Lee A, Oh HG, Yoo YH, Lee J, Kim WT, Lee H. Abiotic Stress-Induced Actin-Depolymerizing Factor 3 From Deschampsia antarctica Enhanced Cold Tolerance When Constitutively Expressed in Rice. Front Plant Sci. 2021; 12:734500.
[5] Lee J, Noh EK, Choi HS, Shin SC, Park H, Lee H. Transcriptome sequencing of the Antarctic vascular plant Deschampsia antarctica Desv. under abiotic stress. Planta. 2013; 237(3):823-36.
[6] Lee J, Kang Y, Shin SC, Park H, Lee H. Combined analysis of the chloroplast genome and transcriptome of the Antarctic vascular plant Deschampsia antarctica Desv. PLoS One. 2014; 9(3):e92501.
[7] Bublyk OM, Andreev IO, Kunakh VA. Bioinformatic prediction of genes of cold-induced transcription factors CBF/DREB1 and DREB4 in Deschampsia antarctica Desv. UAJ. 2016; 15:81-95.
[8] Thomashow MF. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 2010; 154(2):571-7.
[9] Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003; 17(8):1043-54.
[10] Wang DZ, Jin YN, Ding XH, Wang WJ, Zhai SS, Bai LP, Guo ZF. Gene Regulation and Signal Transduction in the ICE-CBF-COR Signaling Pathway during Cold Stress in Plants. Biochemistry (Mosc). 2017; 82(10):1103-1117.
[11] Fursova OV, Pogorelko GV, Tarasov VA. Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene. 2009; 429(1-2):98-103.
[12] Badawi M, Reddy YV, Agharbaoui Z, Tominaga Y, Danyluk J, Sarhan F, Houde M. Structure and functional analysis of wheat ICE (inducer of CBF expression) genes. Plant Cell Physiol. 2008; 49(8):1237-49.
[13] Feng XM, Zhao Q, Zhao LL, Qiao Y, Xie XB, Li HF, Yao YX, You CX, Hao YJ. The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol. 2012; 12:22.
[14] Verma RK, Kumar VVS, Yadav SK, Kumar TS, Rao MV, Chinnusamy V. Overexpression of Arabidopsis ICE1 enhances yield and multiple abiotic stress tolerance in indica rice. Plant Signal Behav. 2020; 15(11):1814547.
[15] Feng HL, Ma NN, Meng X, Zhang S, Wang JR, Chai S, Meng QW. A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco. Plant Physiol Biochem. 2013; 73:309-20.
[16] Li J, Wang L, Zhu W, Wang N, Xin H, Li Sh. Characterization of two VvICE1 genes isolated from 'Muscat Hamburg' grapevine and their effect on the tolerance to abiotic stresses. Sci Hortic. 2014; 165:266-73.
[17] Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell. 2008; 20(7):1775-85.
[18] Lee JH, Jung JH, Park CM. INDUCER OF CBF EXPRESSION 1 integrates cold signals into FLOWERING LOCUS C-mediated flowering pathways in Arabidopsis. Plant J. 2015; 84(1):29-40.
[19] MacGregor DR, Zhang N, Iwasaki M, Chen M, Dave A, Lopez-Molina L, Penfield S. ICE1 and ZOU determine the depth of primary seed dormancy in Arabidopsis independently of their role in endosperm development. Plant J. 2019; 98(2):277-90.
[20] Hu Y, Han X, Yang M, Zhang M, Pan J, Yu D. The Transcription Factor INDUCER OF CBF EXPRESSION1 Interacts with ABSCISIC ACID INSENSITIVE5 and DELLA Proteins to Fine-Tune Abscisic Acid Signaling during Seed Germination in Arabidopsis. Plant Cell. 2019; 31(7):1520-38.
[21] Denay G, Creff A, Moussu S, Wagnon P, Thévenin J, Gérentes MF, Chambrier P, Dubreucq B, Ingram G. Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1. Development. 2014; 141(6):1222-7.
[22] Wei D, Liu M, Chen H, Zheng Y, Liu Y, Wang X, Yang S, Zhou M, Lin J. INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis. PLoS Genet. 2018; 14(10):e1007695.
[23] Kurbidaeva A, Ezhova T, Novokreshchenova M. Arabidopsis thaliana ICE2 gene: phylogeny, structural evolution and functional diversification from ICE1. Plant Sci. 2014; 229:10-22.
[24] Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell. 2007; 19(4):1403-14.
[25] Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK. The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci U S A. 2006; 103(21):8281-6.
[26] Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell. 2015; 32(3):278-89.
[27] Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y. OsMAPK3 Phosphorylates OsbHLH002/OsICE1 and Inhibits Its Ubiquitination to Activate OsTPP1 and Enhances Rice Chilling Tolerance. Dev Cell. 2017; 43(6):731-43.
[28] Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10:421.
[29] Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-9.
[30] Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015; 31(8):1296-7.
[31] Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32(5):1792-7.
[32] Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992; 8(3):275-82.
[33] Nicholas KB, Nicholas HBJ, Deerfield DW. GeneDoc: analysis and visualization of genetic variation. EMBNEW News. 1997; 4:14-6.
[34] Geer LY, Domrachev M, Lipman DJ, Bryant SH. CDART: protein homology by domain architecture. Genome Res. 2002; 12(10):1619-23.
[35] Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Louisville: Humana, 2005. - 571-607 pp.
[36] Chou KC, Shen HB. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One. 2010; 5(6):e11335.
[37] Guo Y, Yang Y, Huang Y, Shen HB. Discovering nuclear targeting signal sequence through protein language learning and multivariate analysis. Anal Biochem. 2020; 591:113565.
[38] Wang D, Liu D, Yuchi J, He F, Jiang Y, Cai S, Li J, Xu D. MusiteDeep: a deep-learning based webserver for protein post-translational modification site prediction and visualization. Nucleic Acids Res. 2020; 48(W1):W140-W146.
[39] Bailey TL, Johnson J, Grant CE, Noble WS. The MEME Suite. Nucleic Acids Res. 2015; 43(W1):W39-49.
[40] Drozdetskiy A, Cole C, Procter J, Barton GJ. JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 2015; 43(W1):W389-94.
[41] Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015; 10(6):845-58.
[42] Ittisoponpisan S, Islam SA, Khanna T, Alhuzimi E, David A, Sternberg MJE. Can Predicted Protein 3D Structures Provide Reliable Insights into whether Missense Variants Are Disease Associated? J Mol Biol. 2019; 431(11):2197-212.
[43] Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002; 30(1):325-7.
[44] Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5(7):621-8.
[45] Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper--Excel-based tool using pair-wise correlations. Biotechnol Lett. 2004; 26(6):509-15.
[46] Rahman MA, Moody MA, Nassuth A. Grape contains 4 ICE genes whose expression includes alternative polyadenylation, leading to transcripts encoding at least 7 different ICE proteins. Environ Exp Bot. 2014; 106:70-8.
[47] Kashyap P, Deswal R. Two ICE isoforms showing differential transcriptional regulation by cold and hormones participate in Brassica juncea cold stress signaling. Gene. 2019; 695:32-41.
[48] Nakamura J, Yuasa T, Huong TT, Harano K, Tanaka S, Iwata T, Phan T, Iwaya M. Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation. Plant Biotechnol. 2011; 28(3):303-9.
[49] Seo H, Sepuru KM, Putarjunan A, Aguirre L, Burrows BA, Torii KU. Intragenic suppressors unravel the role of the SCREAM ACT-like domain for bHLH partner selectivity in stomatal development. Proc Natl Acad Sci U S A. 2022; 119(9):e2117774119.
[50] Staudt AC, Wenkel S. Regulation of protein function by 'microProteins'. EMBO Rep. 2011; 12(1):35-42.
[51] Seo PJ, Hong SY, Kim SG, Park CM. Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci. 2011; 16(10):541-9.
[52] Magnani E, de Klein N, Nam HI, Kim JG, Pham K, Fiume E, Mudgett MB, Rhee SY. A comprehensive analysis of microProteins reveals their potentially widespread mechanism of transcriptional regulation. Plant Physiol. 2014; 165(1):149-59.
[53] Xu Z, Zhou G. Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot. 2008; 59(12):3317-25.
[54] de Oliveira JPV, Duarte VP, de Castro EM, Magalhães PC, Pereira FJ. Stomatal cavity modulates the gas exchange of Sorghum bicolor (L.) Moench. grown under different water levels. Protoplasma. 2022; 259(4):1081-97.
[55] Xu W, Jiao Y, Li R, Zhang N, Xiao D, Ding X, Wang Z. Chinese wild-growing Vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis. PLoS One. 2014; 9(7):e102303.
[56] Deng XM, Wang, JX, Li Y, Wang J, Tian W-M. Characterization of a cold responsive HbICE1 gene from rubber trees. Trees. 2017; 31(1):137-47.
[57] Lu X, Yang L, Yu M, Lai J, Wang C, McNeil D, Zhou M, Yang C. A novel Zea mays ssp. mexicana L. MYC-type ICE-like transcription factor gene ZmmICE1, enhances freezing tolerance in transgenic Arabidopsis thaliana. Plant Physiol Biochem. 2017; 113:78-88.
[58] Jin Y, Zhai S, Wang W, Ding X, Guo Z, Bai L, Wang S. Identification of genes from the ICE-CBF-COR pathway under cold stress in Aegilops-Triticum composite group and the evolution analysis with those from Triticeae. Physiol Mol Biol Plants. 2018; 24(2):211-29.
[59] Zuo ZF, Kang HG, Park MY, Jeong H, Sun HJ, Song PS, Lee HY. Zoysia japonica MYC type transcription factor ZjICE1 regulates cold tolerance in transgenic Arabidopsis. Plant Sci. 2019; 289:110254.
[60] Nakano T, Suzuki K, Fujimura T, Shinshi H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 2006; 140(2):411-32.
[61] Nagashima Y, von Schaewen A, Koiwa H. Function of N-glycosylation in plants. Plant Sci. 2018; 274:70-9.
[62] Luo P, Li Z, Chen W, Xing W, Yang J, Cui Y. Overexpression of RmICE1, a bHLH transcription factor from Rosa multiflora, enhances cold tolerance via modulating ROS levels and activating the expression of stress-responsive genes. Environ Exp Bot. 2020; 178:104160.
[63] Zhang N, McHale LK, Finer JJ. Changes to the core and flanking sequences of G-box elements lead to increases and decreases in gene expression in both native and synthetic soybean promoters. Plant Biotechnol J. 2019; 17(4):724-35.
[64] Gao S, Chu C. Gibberellin Metabolism and Signaling: Targets for Improving Agronomic Performance of Crops. Plant Cell Physiol. 2020; 61(11):1902-11.
[65] Lian TF, Xu YP, Li LF, Su XD. Crystal Structure of Tetrameric Arabidopsis MYC2 Reveals the Mechanism of Enhanced Interaction with DNA. Cell Rep. 2017; 19(7):1334-42.
[66] Anthony-Cahill SJ, Benfield PA, Fairman R, Wasserman ZR, Brenner SL, Stafford WF 3rd, Altenbach C, Hubbell WL, DeGrado WF. Molecular characterization of helix-loop-helix peptides. Science. 1992; 255(5047):979-83.
[67] Feller A, Hernandez JM, Grotewold E. An ACT-like domain participates in the dimerization of several plant basic-helix-loop-helix transcription factors. J Biol Chem. 2006; 281(39):28964-74.
[68] Kong Q, Pattanaik S, Feller A, Werkman JR, Chai C, Wang Y, Grotewold E, Yuan L. Regulatory switch enforced by basic helix-loop-helix and ACT-domain mediated dimerizations of the maize transcription factor R. Proc Natl Acad Sci U S A. 2012; 109(30):E2091-7.
[69] Chipman DM, Shaanan B. The ACT domain family. Curr Opin Struct Biol. 2001; 11(6):694-700.
[70] Guo J, Ren Y, Tang Z, Shi W, Zhou M. Characterization and expression profiling of the ICE-CBF-COR genes in wheat. PeerJ. 2019; 7:e8190.
[71] Man L, Xiang D, Wang L, Zhang W, Wang X, Qi G. Stress-responsive gene RsICE1 from Raphanus sativus increases cold tolerance in rice. Protoplasma. 2017; 254(2):945-56.