Identification and characterization of RuvBL DNA helicase genes for tolerance against abiotic stresses in bread wheat (Triticum aestivum L.) and related species.
Abiotic stress
Helicase
RuvBL
Wheat
Journal
Functional & integrative genomics
ISSN: 1438-7948
Titre abrégé: Funct Integr Genomics
Pays: Germany
ID NLM: 100939343
Informations de publication
Date de publication:
27 Jul 2023
27 Jul 2023
Historique:
received:
02
11
2022
accepted:
13
07
2023
revised:
13
07
2023
medline:
28
7
2023
pubmed:
27
7
2023
entrez:
27
7
2023
Statut:
epublish
Résumé
Recombination UVB (sensitivity) like (RuvBL) helicase genes represent a conserved family of genes, which are known to be involved in providing tolerance against abiotic stresses like heat and drought. We identified nine wheat RuvBL genes, one each on nine different chromosomes, belonging to homoeologous groups 2, 3, and 4. The lengths of genes ranged from 1647 to 2197 bp and exhibited synteny with corresponding genes in related species including Ae. tauschii, Z. mays, O. sativa, H. vulgare, and B. distachyon. The gene sequences were associated with regulatory cis-elements and transposable elements. Two genes, namely TaRuvBL1a-4A and TaRuvBL1a-4B, also carried targets for a widely known miRNA, tae-miR164. Gene ontology revealed that these genes were closely associated with ATP-dependent formation of histone acetyltransferase complex. Analysis of the structure and function of RuvBL proteins revealed that the proteins were localized mainly in the cytoplasm. A representative gene, namely TaRuvBL1a-4A, was also shown to be involved in protein-protein interactions with ten other proteins. On the basis of phylogeny, RuvBL proteins were placed in two sub-divisions, namely RuvBL1 and RuvBL2, which were further classified into clusters and sub-clusters. In silico studies suggested that these genes were differentially expressed under heat/drought. The qRT-PCR analysis confirmed that expression of TaRuvBL genes differed among wheat cultivars, which differed in the level of thermotolerance. The present study advances our understanding of the biological role of wheat RuvBL genes and should help in planning future studies on RuvBL genes in wheat including use of RuvBL genes in breeding thermotolerant wheat cultivars.
Identifiants
pubmed: 37498392
doi: 10.1007/s10142-023-01177-y
pii: 10.1007/s10142-023-01177-y
doi:
Substances chimiques
DNA Helicases
EC 3.6.4.-
DNA, Complementary
0
DNA Transposable Elements
0
RNA, Messenger
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
255Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abdel-Monem M, Durwald H, Hoffmann BH (1976) Enzymic unwinding of DNA: 2. Chain separation by an ATP-dependent DNA unwinding enzyme. Eur J Biochem 65:441–449
pubmed: 133023
Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX:19–25
Abrahao J, Amaro BT, Peres BR, Quel NG, Aragao AZ, Morea EG, Cano MIN, Houry WA, Ramos CH (2021) Leishmania major RUVBL1 has a hexameric conformation in solution and, in the presence of RUVBL2, forms a heterodimer with ATPase activity. Arch Biochem Biophys 703:108841
pubmed: 33775623
Afzal F, Chaudhari SK, Gul A, Farooq A, Ali H, Nisar S, Sarfraz B, Shehzadi KJ, Mujeeb-Kazi A (2015) Bread wheat (Triticum aestivum L.) under biotic and abiotic stresses: an overview. In: Rehman K (ed) Crop production and global environmental issues. Switzerland, Springer International, pp 293–317
Ahmad M, Tuteja R (2012) Plasmodium falciparum RuvB proteins: emerging importance and expectations beyond cell cycle progression. Commun Integr Biol 5:350–361
pubmed: 23060959
pmcid: 3460840
Ahmad M, Afrin F, Tuteja R (2013) Identification of R2TP complex of Leishmania donovani and Plasmodium falciparum using genome wide in-sillico analysis. Commun Integr Biol 6:e26005
pubmed: 24505500
pmcid: 3913666
Ahn S, Anderson JA, Sorrells ME, Tanksley S (1993) Homoeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241:483–490
pubmed: 7903411
Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, Pozniak CJ, Choulet F, Distelfeld A, Poland J (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:7191
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:369–373
Barrier M, Bustamante CD, Yu J, Purugganan MD (2003) Selection on rapidly evolving proteins in the Arabidopsis genome. Genetics 163:723–733
pubmed: 12618409
pmcid: 1462452
Bartos J, Vlcek C, Choulet F, Dzunkova M, Cvikova K, Safar J, Simkova H, Paces J, Strnad H, Sourdille P, Berges H (2012) Intraspecific sequence comparisons reveal similar rates of non-collinear gene insertion in the B and D genomes of bread wheat. BMC Plant Biol 12:1–12
Batra R, Saripalli G, Mohan A, Gupta S, Gill KS, Varadwaj PK, Balyan HS, Gupta PK (2017) Comparative analysis of AGPase genes and encoded proteins in eight monocots and three dicots with emphasis on wheat. Front Plant Sci 8:19
pubmed: 28174576
pmcid: 5259687
Batra R, Agarwal P, Tyagi S, Saini DK, Kumar V, Kumar A, Kumar S, Balyan HS, Pandey R, Gupta PK (2019) A study of CCD8 genes/proteins in seven monocots and eight dicots. PLoS One 14:e0213531
pubmed: 30861026
pmcid: 6413960
Batra R, Gautam T, Pal S, Chaturvedi D, Jan I, Balyan HS, Gupta PK (2020) Identification and characterization of SET domain family genes in bread wheat (Triticum aestivum L.). Sci Rep 10:1–14
Benjak A, Forneck A, Casacuberta JM (2008) Genome-wide analysis of the “Cut-and-Paste” transposons of grapevine. PLoS One 3:e3107
pubmed: 18769592
pmcid: 2528002
Boo K, Bhin J, Jeon Y, Kim J, Shin HJR, Park JE, Kim K, Kim CR, Jang H, Kim IH, Kim VN (2015) Pontin functions as an essential coactivator for Oct4-dependent lincRNA expression in mouse embryonic stem cells. Nat Commun 6:1–16
Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436:282–284
pubmed: 16015335
Calvi BR, Hong TJ, Findley SD, Gelbart WM (1991) Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell 66:465–471
pubmed: 1651170
Cavrak VV, Lettner N, Jamge S, Kosarewicz A, Bayer LM, Scheid OM (2014) How a retrotransposon exploits the plant's heat stress response for its activation. PLoS Genet 10:e1004115
pubmed: 24497839
pmcid: 3907296
Chen N (2004) Using Repeat Masker to identify repetitive elements in genomic sequences. Curr Protoc Bioinform 5:4–10
Chen Y, Liu T, Tian X, Wang X, Li M, Wang S, Wang Z (2015) Effects of plastic film combined with straw mulch on grain yield and water use efficiency of winter wheat in Loess Plateau. Field Crops Res 172:53–58
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 13:1194–1202
pubmed: 32585190
Cheung KL, Huen J, Kakihara Y, Houry WA, Ortega J (2010) Alternative oligomeric states of the yeast Rvb1/Rvb2 complex induced by histidine tags. J Mol Biol 404:478–492
pubmed: 20934430
pmcid: 2982833
Choi J, Heo K, An W (2009) Cooperative action of TIP48 and TIP49 in H2A. Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res 37:5993–6007
pubmed: 19696079
pmcid: 2764430
Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519
pubmed: 8401235
pmcid: 2142462
Cork JM, Purugganan MD (2005) High-diversity genes in the Arabidopsis genome. Genetics 170:1897–1911
pubmed: 15911589
pmcid: 1449776
Cunningham F, Allen JE, Allen J, Jarreta JA, Amode MR, Armean IM, Austine-Orimoloye O, Azov AG, Barnes I, Bennett R, Berry A (2022) Ensembl 2022. Nucleic Acids Res 50:988–995
Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46:49–54
Dang HQ, Tran NQ, Gill SS, Tuteja R, Tuteja N (2011) A single subunit MCM6 from pea promotes salinity stress tolerance without affecting yield. Plant Mol Biol 76:19–34
pubmed: 21365356
Dawid A, Croquette V, Grigoriev M, Heslot F (2004) Single-molecule study of RuvAB-mediated holliday-junction migration. Proc Natl Acad Sci USA 101:11611–11616
pubmed: 15292508
pmcid: 511028
De Felice B, Wilson RR, Argenziano C, Kafantaris I, Conicella C (2009) A transcriptionally active copia-like retroelement in Citrus limon. Cell Mol Biol Lett 14:289–304
pubmed: 19115051
Devos KM, Dubcovsky J, Dvorak J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91:282–288
pubmed: 24169776
Ding S, Cai Z, Du H, Wang H (2019) Genome-wide analysis of TCP family genes in Zea mays L. identified a role for ZmTCP42 in drought tolerance. Int J Mol 20:2762
Dvorak J, Yang ZL, You FM, Luo MC (2004) Deletion polymorphism in wheat chromosome regions with contrasting recombination rates. Genetics 168(3):1665–1675
pubmed: 15579715
pmcid: 1448774
Dvorak J, Wang L, Zhu T, Jorgensen CM, Luo MC, Deal KR, Gu YQ, Gill BS, Distelfeld A, Devos KM, Qi P (2018) Reassessment of the evolution of wheat chromosomes 4A, 5A, and 7B. Theor Appl Genet 131:2451–2462
pubmed: 30141064
pmcid: 6208953
Eckardt NA (2003) Maize genetics 2003. Plant Cell 15:1053–1055
pubmed: 12724532
pmcid: 526039
Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404
pubmed: 9379925
Endo T, Ikeo K, Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685–690
pubmed: 8676743
Feng H, Duan X, Zhang Q, Li X, Wang B, Huang L, Wang X, Kang Z (2014) The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Mol Plant Pathol 15:284–296
pubmed: 24128392
pmcid: 6638668
Fritsch O, Benvenuto G, Bowler C, Molinier J, Hohn B (2004) The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol Cell 16:479–485
pubmed: 15525519
Gamboatuz SD, Pereirasantana A, Zamorabriseno JA (2018) Transcriptomics and co-expression networks reveal tissue-specific responses and regulatory hubs under mild and severe drought in papaya (Carica papaya L.). Sci. Rep. 8:14539
pubmed: 30267030
Garg VK, Avashthi H, Tiwari A, Jain PA, Ramkete PW, Kayastha AM, Singh VK (2016) MFPPI–multi FASTA ProtParam Interface. Bioinformation 12:74–77
pubmed: 28104964
pmcid: 5237651
Garnier J, Gibrat JF, Robson B (1996) GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 266:540–553
pubmed: 8743705
Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809–6814
pubmed: 11038553
pmcid: 21240
Gill BS, Appels R, Oberholster AMB, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorak J, Iwanaga M, Keller B, Li W (2004) A workshop report on wheat genome sequencing: International Genome Research on Wheat Consortium. Genetics 168:1087–1096
pubmed: 15514080
pmcid: 1448818
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186
Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17:4713–4730
pubmed: 2546125
pmcid: 318027
Gribun A, Cheung KL, Huen J, Ortega J, Houry WA (2008) Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. J Mol Biol 376:1320–1333
pubmed: 18234224
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agricultural Exp Station 347(2):32
Hollender CA, Kang CY, Darwish O, Geretz A, Matthews BF, Slovin J, Alkharouf N, Liu ZC (2014) Floral transcriptomes in woodland strawberry uncover developing receptacle and anther gene networks. Plant Physiol 165:1062–1075
Holt BF, Boyes DC, Ellerstrom M, Siefers N, Wiig A, Kauffman S, Grant MR, Dangl JL (2002) An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev Cell 2:807–817
pubmed: 12062092
Huang C, Sun H, Xu D, Chen Q, Liang Y, Wang X, Xu G, Tian J, Wang C, Li D, Wu L (2018) ZmCCT9 enhances maize adaptation to higher latitudes. Proc Natl Acad Sci USA 115:E334–E341
pubmed: 29279404
Ikai A (1980) Thermostability and aliphatic index of globular proteins. J Biochem 88:1895–1898
pubmed: 7462208
International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J, Pozniak CJ, Choulet F, Distelfeld A, Poland J (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:7191
Jesus EMD, Ochoa Cruz EA, Cruz GM, Van Sluys MA (2012) Diversification of hAT transposase paralogues in the sugarcane genome. Mol Genet Genom 287:205–219
Jiao Y, Deng XW (2007) A genome-wide transcriptional activity survey of rice transposable element-related genes. Genome Biol 8:1–19
Joo J, Lee YH, Kim YK, Nahm BH, Song SI (2013) Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue-dependent sugar and hormone-sensitivities. Mol Cells 35:421–435
pubmed: 23620302
pmcid: 3887869
Ke Q, Sun H, Tang M, Luo R, Zeng Y, Wang M, Li Y, Li Z, Cui L (2022) Genome-wide identification, expression analysis and evolutionary relationships of the IQ67-domain gene family in common wheat (Triticum aestivum L.) and its progenitors. BMC genomics 23:264
pubmed: 35382737
pmcid: 8981769
Knoll A, Puchta H (2011) The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. J Exp Bot 62:1565–1579
pubmed: 21081662
Kumar A, Batra R, Gahlaut V, Gautam T, Kumar S, Sharma M, Tyagi S, Singh KP, Balyan HS, Pandey R, Gupta PK (2018) Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.). PLoS One 13:e0208409
pubmed: 30540790
pmcid: 6291158
Kumar R, Masthigowda MH, Kaur A, Bhusal N, Pandey A, Kumar S, Mishra C, Singh G, Singh GP (2020) Identification and characterization of multiple abiotic stress tolerance genes in wheat. Mol Biol Rep 47:8629–8643
pubmed: 33068231
Kumar S, Singh VP, Saini DK, Sharma H, Saripalli G, Kumar S, Balyan HS, Gupta PK (2021) Meta-QTLs, ortho-MQTLs, and candidate genes for thermotolerance in wheat (Triticum aestivum L.). Mol Breeding 41:1–22
Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK - a program to check the stereochemical quality of protein structures. J App Cryst 26:283–291
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Peer YVD, 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 30:325–327
pubmed: 11752327
pmcid: 99092
Li WH (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitutions. J Mol Evol. 36:96–99
pubmed: 8433381
Liberles D, Schreiber D, Govindarajan S, Chamberlin S, Benner S (2001) The Adaptive Evolution Database (TAED). Genome Biol 2:28
Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61
pubmed: 23247435
Liu X, Inoue H, Tang X, Tan Y, Xu X, Wang C, Jiang CJ (2020) Rice OsAAA-ATPase1 is induced during blast infection in a salicylic acid-dependent manner, and Promotes blast fungus resistance. Int J Mol Sci 21:1443
pubmed: 32093321
pmcid: 7073101
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
pubmed: 11846609
Lv L, Zhang W, Sun L, Zhao A, Zhang Y, Wang L, Liu Y, Li Z, Li H, Chen X (2020) Gene co-expression network analysis to identify critical modules and candidate genes of drought-resistance in wheat. PLoS One 15:8
Ma J, Li R, Wang H, Li D, Wang X, Zhang Y, Zhen W, Duan H, Yan G, Li Y (2017) Transcriptomics analyses reveal wheat responses to drought stress during reproductive stages under field conditions. Front Plant Sci 8:592
pubmed: 28484474
pmcid: 5399029
Ma S, Wang M, Wu J, Guo W, Chen Y, Li G, Wang Y, Shi W, Xia G, Fu D, Kang Z (2021) WheatOmics: a platform combining multiple omics data to accelerate functional genomics studies in wheat. Mol Plant. 14:1965–1968
pubmed: 34715393
Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ibarra JR, Springer NM (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11:e1004915
pubmed: 25569788
pmcid: 4287451
Manova V, Gruszka D (2015) DNA damage and repair in plants–from models to crops. Front Plant Sci 6:885
pubmed: 26557130
pmcid: 4617055
Marchler-bauer M, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:200–203
Matias PM, Gorynia S, Donner P, Carrondo MA (2006) Crystal structure of the human AAA+ protein RuvBL1. J Biol Chem 281:38918–38929
pubmed: 17060327
Morrison AJ (2017) Genome maintenance functions of the INO80 chromatin remodeller. Philos Trans R Soc Lond B Biol Sci 372:20160289
pubmed: 28847826
pmcid: 5577467
Nakashima K, Shinozaki KY, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170
pubmed: 24904597
pmcid: 4032904
Passricha N, Saifi SK, Gill SS, Tuteja R, Tuteja N (2019) Role of plant helicases in imparting salinity stress tolerance to plants. In: Tuteja R (ed) helicases from all domains of life. eBook Academic Press, pp 39–52. https://doi.org/10.1016/B978-0-12-814685-9.00003-8
Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M, Sonah H, Song L, Lin L, Chaudhary J, Liu Y (2015) Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. Bmc Genomics 16:1–16
Paz I, Kligun E, Bengad B, Gutfreund YM (2016) BindUP: a web server for non-homology-based prediction of DNA and RNA binding proteins. Nucleic Acids Res 44:568–574
Punta M, Coggil PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A (2012) The Pfam protein families database. Nucleic Acids Res. 40(D1):D290–D301
pubmed: 22127870
Putnam CD, Clancy SB, Tsuruta H, Gonzalez S, Wetmur JG, Tainer JA (2001) Structure and mechanism of the RuvB Holliday junction branch migration motor. J Mol Biol 311:297–310
pubmed: 11478862
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:116–120
Ritchie DW, Kemp GJ (2000) Protein docking using spherical polar Fourier correlations. Proteins: Struct. Funct. Genet. 39:178–194
Roberts WR, Roalson EH (2017) Comparative transcriptome analyses of flower development in four species of Achimenes (Gesneriaceae). BMC Genomics 18:240
pubmed: 28320315
pmcid: 5359931
Roth C, Liberles DA (2006) A systematic search for positive selection in higher plants (Embryophytes). BMC Plant Biol. 6:12
pubmed: 16784532
pmcid: 1540423
Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957
pubmed: 11454746
pmcid: 1461711
Saifi SK, Passricha N, Swain DM, Tuteja N (2017) Prediction of cis-regulatory elements for a detailed insight of RuvB family genes from Oryza sativa. Oryza-Int J Rice 54:135–147
Saifi SK, Passricha N, Tuteja R, Tuteja N (2018) Stress-induced Oryza sativa RuvBL1a is DNA-independent ATPase and unwinds DNA duplex in 3′ to 5′ direction. Protoplasma 255:669–684
pubmed: 29103092
Saifi SK, Passricha N, Tuteja R, Tuteja N (2019) An overview of AAA + superfamily proteins associated helicases. In: Tuteja R (ed) Helicases from all domains of life. Academic Press, pp 247–264
Saifi SK, Passricha N, Tuteja R, Nath M, Gill SS, Tuteja N (2021) OsRuvBL1a DNA helicase boost salinity and drought tolerance in transgenic indica rice raised by in-planta transformation. Res Sq. https://doi.org/10.21203/rs.3.rs-405060/v1
Schmid SR, Linder P (1992) D-E-A-D protein family of putative RNA helicases. Mol Microbiol 6:283–291
pubmed: 1552844
Schorova S, Fajkus J, Drabkova LZ, Honys D, Schrumpfova PP (2019) The plant Pontin and Reptin homologues, RuvBL1 and RuvBL2a, colocalize with TERT and TRB proteins in vivo, and participate in telomerase biogenesis. Plant J 98:195–212
pubmed: 30834599
Shi L, Song J, Guo C, Wang B, Guan Z, Yang P, Chen X, Zhang Q, King GJ, Wang J, Liu K (2019) A CACTA-like transposable element in the upstream region of BnaA9.CYP78A9 acts as an enhancer to increase silique length and seed weight in rapeseed. Plant J 98:524–539
pubmed: 30664290
Shivakumara TN, Sreevathsa R, Dash PK, Sheshshayee MS, Papolu PK, Rao U, Tuteja N, UdayaKumar M (2017) Overexpression of pea DNA helicase 45 (PDH45) imparts tolerance to multiple abiotic stresses in chili (Capsicum annuum L.). Sci Rep 7:1–12
Simonetti FL, Teppa E, Chernomoretz A, Nielsen M, Buslje CM (2013) MISTIC: mutual information server to infer coevolution. Nucleic Acids Res 41:8–14
Singh R, Sharma S, Kharb P, Saifi S, Tuteja N (2020) OsRuvB transgene induces salt tolerance in pigeon pea. J Plant Interact 15:17–26
Snider J, Thibault G, Houry WA (2008) The AAA+ superfamily of functionally diverse proteins. Genome Biol 9:1–8
Solangi AH, Solongi N, Jatoi WA, Solangi MK, Solangi SK, Memom S, Halepoto AG, Kumbhar S, Soomro S (2021) Drought tolerance indices of wheat (Triticum aestivum L.) genotypes under water deficit conditions. Plant Cell Biotechnol Mol Biol 22:1–19
Sorrells ME, Rota ML, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Mahmoud A, Ma X, Gustafson PJ, Qi LL, Echalier B (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827
pubmed: 12902377
pmcid: 403773
Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) On the tetraploid origin of the maize genome. Comp Funct Genom 5:281–284
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:607–613
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
pubmed: 33892491
pmcid: 8233496
Tanin MJ, Saini DK, Sandhu KS, Pal N, Gudi S, Chaudhary J, Sharma A (2022) Consensus genomic regions associated with multiple abiotic stress tolerance in wheat and implications for wheat breeding. Sci. Rep 12:13680
pubmed: 35953529
pmcid: 9372038
Thompson JD, Gibson TJ, Higgins DG (2003) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform 1:2–3
Thomsen R, Christensen MH (2006) MolDock: a new technique for high-accuracy molecular docking. J Med Chem 49:3315–3321
pubmed: 16722650
Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681:134–149
pubmed: 18652913
Tuteja N, Banu MSA, Huda KMK, Gill SS, Jain P, Pham XH, Tuteja R (2014) Pea p68, a DEAD-box helicase, provides salinity stress tolerance in transgenic tobacco by reducing oxidative stress and improving photosynthesis machinery. PloS One 9:e98287
pubmed: 24879307
pmcid: 4039504
Tuteja N, Tarique M, Trivedi DK, Sahoo RK, Tuteja R (2015) Stress-induced Oryza sativa BAT1 dual helicase exhibits unique bipolar translocation. Protoplasma 252:1563–1574
pubmed: 25772680
Utley RT, Lacoste N, Robitaille OJ, Allard S, Cote J (2005) Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol Cell Biol 25:8179–8190
pubmed: 16135807
pmcid: 1234332
Wang CW, Chen WC, Lin LJ, Lee CT, Tseng TH, Leu WM (2011) OIP30, a RuvB-like DNA helicase 2, is a potential substrate for the pollen-predominant OsCPK25/26 in rice. Plant Cell Physiol 52:1641–1656
pubmed: 21771866
Wang Z, Zhao G, Yang Q, Gao L, Liu C, Ru Z, Wang D, Jia J, Cui D (2022) Helitron and CACTA DNA transposons actively reshape the common wheat-AK58 genome. Genomics 114:110288
pubmed: 35124171
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, Beer TAPD, Rempfer C, Bordoli L, Lepore R (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:296–303
Wiedemann G, Gessel NV, Köchl F, Hunn L, Schulze K, Maloukh L, Nogue F, Decker EL, Hartung F, Reski R (2018) RecQ helicases function in development, DNA repair, and gene targeting in Physcomitrella patens. Plant Cell 30:717–736
pubmed: 29514942
pmcid: 5894843
Yamada K, Kunishima N, Mayanagi K, Ohnishi T, Nishino T, Iwasaki H, Shinagawa H, Morikawa K (2001) Crystal structure of the holliday junction migration motor protein RuvB from Thermus thermophilus HB8. Proc Natl Acids Sci USA 98:1442–1447
Yang Z, Bielawski J (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503
pubmed: 11114436
pmcid: 7134603
Ye Y, Godzik A (2004) FATCAT: a web server for flexible structure comparison and structure similarity searching. Nucleic Acids Res 32:W582–W585
pubmed: 15215455
pmcid: 441568
Zampieri M, Ceglar A, Dentener F, Toreti A (2017) Wheat yield loss attributable to heat waves, drought and water excess at the global, national and subnational scales. Environ Res Lett 12:064008
Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Gen Mol Biol 4:17. https://doi.org/10.2202/1544-6115.1128
Zhang P, Zang Y, Sun L, Sinumporn S, Yang Z, Sun B, Xuan D, Li Z, Yu P, Wu W, Wang K (2017a) The rice AAA-ATPase OsFIGNL1 is essential for male meiosis. Front Plant Sci 8:1639
pubmed: 29021797
pmcid: 5624289
Zhang Y, Pan J, Huang X, Guo D, Lou H, Hou Z, Su M, Liang R, Xie C, You M, Li B (2017b) Differential effects of a post-anthesis heat stress on wheat (Triticum aestivum L.) grain proteome determined by iTRAQ. Sci Rep 7:1–11
Zheng J, He C, Qin Y, Lin G, Park WD, Sun M et al (2019) Co-expression analysis aids in the identification of genes in the cuticular wax pathway in maize. Cell Mol Biol 97:530
Zhou X, Zhu X, Shao W, Song J, Jiang W, He Y, Yin J, Ma D, Qiao Y (2020) Genome-wide mining of wheat DUF966 gene family provides new insights into salt stress responses. Front Plant Sci 11:569838
pubmed: 32983219
pmcid: 7483657