Abstract
The ATP-binding cassette (ABC) transporter family is one of the largest protein families in plants and plays an essential role in addressing biotic and abiotic stresses. Wheat, a vital global grain crop, faces multifaceted safety challenges, primarily from fungal diseases like stripe rust and powdery mildew. In the present study, we identified the whole genome of the wheat ABC family, and 463 nonredundant ABC genes were identified. The ABC family can be divided into nine evolutionary branches and eight subfamilies based on phylogenetic tree analysis. This paper delved deeper into characterizing the gene structure, promoter region, and gene expression within the TaABC family. Segmental duplication was the main reason for the expansion of the TaABC genes. Ka/Ks analysis suggested that most TaABC genes were intensely purified and selected. The collinear analysis of TaABC and other species showed that the ABC genes were conserved in evolution. RNA-seq data and qPCR data from wheat infected with powdery mildew or stripe rust showed that most TaABC genes were induced to change expression. The candidate genes TaABCB15-3B and TaABCG38 exhibited responsiveness to powdery mildew in resistant/susceptible wheat, while remaining unresponsive to stripe rust. Our findings serve as a valuable reference for gaining a deeper understanding of the function and evolution of TaABCs, aiding in the identification of enduring disease resistance genes within the TaABCs of wheat.
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Data availability
NCBI publicly available datasets were analyzed in this study. These data can be found here PRJNA243835, PRJNA387101, PRJNA472848, PRJNA613349, PRJNA637808, and PRJNA401295. All data generated or analyzed during this study are included in this published article and the additional files.
Abbreviations
- Pst :
-
Puccinia striiformis F. sp. tritici Eriks
- Bgt :
-
Blumeria graminis F. sp. tritici
- ABC:
-
ATP-binding cassette
- MeJA:
-
Methyl jasmonate
- ABA:
-
Abscisic acid
- MYB:
-
Myeloblastosis
- TMDs:
-
Transmembrane domains
- NBDs:
-
Nucleotide-binding domains
- Ka:
-
The non-synonymous substitution rate
- Ks:
-
The synonymous substitution rate
- Ta:
-
Triticum aestivum L.
- DON:
-
Deoxynivalenol
- JA:
-
Jasmonic acid
- PEN:
-
PENETRATION
- MYA:
-
Millions years ago
- FPKM:
-
Fragments per kilobase of exon model per million mapped fragments
References
Badouin H, Gouzy J, Grassa CJ, Murat F, Staton SE, Cottret L, Lelandais-Brière C, Owens GL, Carrère S, Mayjonade B et al (2017) The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546:148–152. https://doi.org/10.1038/nature22380
Banasiak J, Jasinski M (2022) ATP-binding cassette transporters in nonmodel plants. New Phytol. https://doi.org/10.1111/nph.17779
Bessire M, Borel S, Fabre G, Carraça L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Métraux JP, Nawrath C (2011) A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23:1958–1970. https://doi.org/10.1105/tpc.111.083121
Bhati KK, Sharma S, Aggarwal S, Kaur M, Shukla V, Kaur J, Mantri S, Pandey AK (2015) Genome-wide identification and expression characterization of ABCC-MRP transporters in hexaploid wheat. Front Plant Sci 6:488. https://doi.org/10.3389/fpls.2015.00488
Biala W, Banasiak J, Jarzyniak K, Pawela A, Jasinski M (2017) Medicago truncatula ABCG10 is a transporter of 4-coumarate and liquiritigenin in the medicarpin biosynthetic pathway. J Exp Bot 68:3231–3241. https://doi.org/10.1093/jxb/erx059
Bolton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575. https://doi.org/10.1111/j.1364-3703.2008.00487.x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen S, Ren C, Zhai J, Yu J, Zhao X, Li Z, Zhang T, Ma W, Han Z, Ma C (2020b) CAFU: a Galaxy framework for exploring unmapped RNA-Seq data. Brief Bio 21:676–686. https://doi.org/10.1093/bib/bbz018
Clark JW, Donoghue PCJ (2018) Whole-genome duplication and plant macroevolution. Trends Plant Sci 23:933–945. https://doi.org/10.1016/j.tplants.2018.07.006
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101. https://doi.org/10.1126/science.1164627
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122
Dassa E, Bouige P (2001) The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152:211–229. https://doi.org/10.1016/s0923-2508(01)01194-9
Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364. https://doi.org/10.1128/MMBR.00031-07
Dean M, Hamon Y, Chimini G (2001) The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 42:1007–1017
Dejonghe W, Okamoto M, Cutler SR (2018) Small Molecule probes of ABA biosynthesis and signaling. Plant Cell Physiol 59:1490–1499. https://doi.org/10.1093/pcp/pcy126
Dong Q, Magwanga RO, Cai X, Lu P, Nyangasi Kirungu J, Zhou Z, Wang X, Wang X, Xu Y, Hou Y et al (2019) RNA-sequencing, physiological and RNAi analyses provide insights into the response mechanism of the ABC-mediated resistance to Verticillium dahliae Infection in Cotton. Genes 20:10–15. https://doi.org/10.3390/genes10020110
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Feng Y, Sun Q, Zhang G, Wu T, Zhang X, Xu X, Han Z, Wang Y (2019) Genome-wide identification and characterization of ABC transporters in nine rosaceae species identifying MdABCG28 as a possible cytokinin transporter linked to dwarfing. Int J Mol Sci. https://doi.org/10.3390/ijms20225783
Francisco RM, Regalado A, Ageorges A, Burla BJ, Bassin B, Eisenach C, Zarrouk O, Vialet S, Marlin T, Chaves MM et al (2013) ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-Glucosides. Plant Cell 25:1840–1854. https://doi.org/10.1105/tpc.112.102152
Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249–265. https://doi.org/10.1016/j.jmb.2004.07.093
Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL et al (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194. https://doi.org/10.1111/j.1365-313X.2005.02519.x
George AM, Jones PM (2012) Perspectives on the structure-function of ABC transporters: the switch and constant contact models. Prog Biophys Mol Biol 109:95–107. https://doi.org/10.1016/j.pbiomolbio.2012.06.003
Griffey CA, Das MK, Stromberg EL (1993) Effectiveness of adult-plant resistance in reducing grain yield loss to powdery mildew in winter wheat. Plant Dis 77:618–622
Higgins CF, Linton KJ (2004) The ATP switch model for ABC transporters. Nat Struct 11:918–926. https://doi.org/10.1038/nsmb836
Hu Y, Liang Y, Zhang M, Tan F, Zhong S, Li X, Gong G, Chang X, Shang J, Tang S et al (2018) Comparative transcriptome profiling of Blumeria graminis f. sp. tritici during compatible and incompatible interactions with sister wheat lines carrying and lacking Pm40. PLoS One 13:e0198891–e0198891. https://doi.org/10.1371/journal.pone.0198891
Hu Y, Zhong S, Zhang M, Liang Y, Gong G, Chang X, Tan F, Yang H, Qiu X, Luo L, Luo P (2020) Potential role of photosynthesis in the regulation of reactive oxygen species and defence responses to Blumeria graminis f. sp. tritici in wheat. Int J Mol Sci 21:5767. https://doi.org/10.3390/ijms21165767
Huang J, Li X, Chen X, Guo Y, Liang W, Wang H (2021) Genome-wide identification of soybean ABC transporters relate to aluminum toxicity. Int J Mol Sci. https://doi.org/10.3390/ijms22126556
Hwang JU, Song WY, Hong D, Ko D, Yamaoka Y, Jang S, Yim S, Lee E, Khare D, Kim K et al (2016) Plant ABC transporters enable many unique aspects of a terrestrial plant’s lifestyle. Mol Plant 9:338–355. https://doi.org/10.1016/j.molp.2016.02.003
Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100. https://doi.org/10.1038/nature09916
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. PNAS 107:2355–2360. https://doi.org/10.1073/pnas.0909222107
Khan N, You FM, Datla R, Ravichandran S, Jia B, Cloutier S (2020) Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L.). BMC Genomics 21:722. https://doi.org/10.1186/s12864-020-07121-9
Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song WY et al (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. PNAS 111:7150–7155. https://doi.org/10.1073/pnas.1321519111
Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318. https://doi.org/10.1093/pcp/pcj001
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363. https://doi.org/10.1126/science.1166453
Krattinger SG, Kang J, Bräunlich S, Boni R, Chauhan H, Selter LL, Robinson MD, Schmid MW, Wiederhold E, Hensel G et al (2019) Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytol 223:853–866. https://doi.org/10.1111/nph.15815
Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344. https://doi.org/10.1038/nature10873
Lane TS, Rempe CS, Davitt J, Staton ME, Peng Y, Soltis DE, Melkonian M, Deyholos M, Leebens-Mack JH, Chase M et al (2016) Diversity of ABC transporter genes across the plant kingdom and their potential utility in biotechnology. BMC Biotechnol 16:47. https://doi.org/10.1186/s12896-016-0277-6
Liang Z, Schnable JC (2018) Functional divergence between subgenomes and gene pairs after whole genome duplications. Mol Plant 11:388–397. https://doi.org/10.1016/j.molp.2017.12.010
Lopez-Ortiz C, Dutta SK, Natarajan P, Peña-Garcia Y, Abburi V, Saminathan T, Nimmakayala P, Reddy UK (2019) Genome-wide identification and gene expression pattern of ABC transporter gene family in Capsicum spp. PLoS One 14:e0215901. https://doi.org/10.1371/journal.pone.0215901
Matern A, Böttcher C, Eschen-Lippold L, Westermann B, Smolka U, Döll S, Trempel F, Aryal B, Scheel D, Geisler M, Rosahl S (2019) A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana. J Biol Chem 294:6857–6870. https://doi.org/10.1074/jbc.RA119.007676
McFarlane HE, Shin JJ, Bird DA, Samuels AL (2010) Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22:3066–3075. https://doi.org/10.1105/tpc.110.077974
Michieli M, Damiani D, Geromin A, Michelutti A, Fanin R, Raspadori D, Russo D, Visani G, Dinota A, Pileri S et al (1992) Overexpression of multidrug resistance-associated p170-glycoprotein in acute non-lymphocytic leukemia. Eur J Haematol 48:87–92. https://doi.org/10.1111/j.1600-0609.1992.tb00571.x
Mishra AK, Choi J, Rabbee MF, Baek KH (2019) In silico genome-wide analysis of the ATP-binding cassette transporter gene family in soybean (Glycine max L.) and their expression profiling. Biomed Res Int 2019:8150523. https://doi.org/10.1155/2019/8150523
Ofori PA, Mizuno A, Suzuki M, Martinoia E, Reuscher S, Aoki K, Shibata D, Otagaki S, Matsumoto S, Shiratake K (2018) Genome-wide analysis of ATP binding cassette (ABC) transporters in tomato. PLoS One 13:e0200854. https://doi.org/10.1371/journal.pone.0200854
One thousand plant transcriptomes and the phylogenomics of green plants. (2019) Nature 574(7780):679–685. https://doi.org/10.1038/s41586-019-1693-2
Pang K, Li Y, Liu M, Meng Z, Yu Y (2013) Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526:411–428. https://doi.org/10.1016/j.gene.2013.05.051
Panikashvili D, Shi JX, Schreiber L, Aharoni A (2011) The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol 190:113–124. https://doi.org/10.1111/j.1469-8137.2010.03608.x
Peng FY, Yang RC (2017) Prediction and analysis of three gene families related to leaf rust (Puccinia triticina) resistance in wheat (Triticum aestivum L.). BMC Plant Biol 17:108. https://doi.org/10.1186/s12870-017-1056-9
Pradhan AK, Kumar S, Singh AK, Budhlakoti N, Mishra DC, Chauhan D, Mittal S, Grover M, Kumar S, Gangwar OP et al (2020) Identification of QTLs/defense genes effective at seedling stage against prevailing races of wheat stripe rust in India. Front Genet 11:572975–572975. https://doi.org/10.3389/fgene.2020.572975
Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J (2018) Widespread whole genome duplications contribute to genome complexity and species diversity in Angiosperms. Mol Plant 11:414–428. https://doi.org/10.1016/j.molp.2018.01.002
Rin S, Mizuno Y, Shibata Y, Fushimi M, Katou S, Sato I, Chiba S, Kawakita K, Takemoto D (2017) EIN2-mediated signaling is involved in pre-invasion defense in Nicotiana benthamiana against potato late blight pathogen, phytophthora infestans. Plant Signal Behav 12:e1300733. https://doi.org/10.1080/15592324.2017.1300733
Saha J, Sengupta A, Gupta K, Gupta B (2015) Molecular phylogenetic study and expression analysis of ATP-binding cassette transporter gene family in Oryza sativa in response to salt stress. Comput Biol Chem 54:18–32. https://doi.org/10.1016/j.compbiolchem.2014.11.005
Sanchez-Fernandez R, Davies TG, Coleman JO, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244. https://doi.org/10.1074/jbc.M103104200
Sanchez-Vallet A, Ramos B, Bednarek P, López G, Piślewska-Bednarek M, Schulze-Lefert P, Molina A (2010) Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63:115–127. https://doi.org/10.1111/j.1365-313X.2010.04224.x
Schwager EE, Sharma PP, Clarke T, Leite DJ, Wierschin T, Pechmann M, Akiyama-Oda Y, Esposito L, Bechsgaard J, Bilde T et al (2017) The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biol 15:62. https://doi.org/10.1186/s12915-017-0399-x
Segraves KA (2017) The effects of genome duplications in a community context. New Phytol 215:57–69. https://doi.org/10.1111/nph.14564
Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. PNAS 100:751–756. https://doi.org/10.1073/pnas.0134257100
Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746. https://doi.org/10.1105/tpc.105.038372
Sugiyama A, Shitan N, Sato S, Nakamura Y, Tabata S, Yazaki K (2006) Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus: comparison with Arabidopsis ABC protein family. DNA Res 13:205–228. https://doi.org/10.1093/dnares/dsl013
Tucker JR, Legge WG, Maiti S, Hiebert CW, Simsek S, Yao Z, Xu W, Badea A, Fernando WGD (2021) Transcriptome alterations of an in vitro-selected, moderately resistant, two-row malting barley in response to 3ADON, 15ADON, and NIV chemotypes of Fusarium graminearum. Front Plant Sci 12:701969. https://doi.org/10.3389/fpls.2021.701969
Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E et al (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159. https://doi.org/10.1016/j.tplants.2008.02.001
Walter S, Brennan JM, Arunachalam C, Ansari KI, Hu X, Khan MR, Trognitz F, Trognitz B, Leonard G, Egan D, Doohan FM (2008) Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol. Funct Integr Genomic 8:421–427. https://doi.org/10.1007/s10142-008-0089-4
Walter S, Kahla A, Arunachalam C, Perochon A, Khan MR, Scofield SR, Doohan FM (2015) A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. J Exp Bot 66:2583–2593. https://doi.org/10.1093/jxb/erv048
Wang S, Li L, Li H, Sahu SK, Wang H, Xu Y, Xian W, Song B, Liang H, Cheng S et al (2020) Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nature Plants 6:95–106. https://doi.org/10.1038/s41477-019-0560-3
Wellings CR (2011) Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–141. https://doi.org/10.1007/s10681-011-0360-y
Yan C, Duan W, Lyu S, Li Y, Hou X (2017) Genome-wide identification, evolution, and expression analysis of the ATP-binding cassette transporter gene family in Brassica rapa. Front Plant Sci 8:349. https://doi.org/10.3389/fpls.2017.00349
Zhang H, Yang Y, Wang C, Liu M, Li H, Fu Y, Wang Y, Nie Y, Liu X, Ji W (2014) Large-scale transcriptome comparison reveals distinct gene activations in wheat responding to stripe rust and powdery mildew. BMC Genomics 15:898–898. https://doi.org/10.1186/1471-2164-15-898
Zhang XD, Zhao KX, Yang ZM (2018) Identification of genomic ATP binding cassette (ABC) transporter genes and Cd-responsive ABCs in Brassica napus. Gene 664:139–151. https://doi.org/10.1016/j.gene.2018.04.060
Acknowledgements
The authors would like to thank Guorong Wei, Senior laboratory Technician of Plant Protection College of Northwest A&F University, for providing us with stripe rust fungus.
Funding
This research was funded by the Shaanxi Research Station of Crop Gene Resources and Germplasm Enhancement Program of China (No. Z100021811), National Natural Science Foundation of China (31971741) and the Shaanxi Innovation Team Project (2018TD-004), Germplasm Innovation and Breakthrough Cultivar Breeding of Wheat.
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Conceptualization: WJ and HZ; methodology: GW; software: GW and DL; validation: WJ, CC and HZ; formal analysis: GW and XZ; investigation: GW, XZ and CZ; resources: CC; data curation: GW; writing—original draft preparation: GW; writing—review and editing: JG; visualization: GW and JG; supervision: HZ; project administration: CC; funding acquisition: WJ and CC. All authors have read and agreed to the published version of the manuscript.
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Wang, G., Gu, J., Long, D. et al. Genome-wide identification of wheat ABC gene family and expression in response to fungal stress treatment. Plant Biotechnol Rep (2023). https://doi.org/10.1007/s11816-023-00881-2
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DOI: https://doi.org/10.1007/s11816-023-00881-2