Comprehensive genome-wide analysis of wheat xylanase inhibitor protein (XIP) genes: unveiling their role in Fusarium head blight resistance and plant immune mechanisms.
Crop breeding strategies
Fungal disease management
Gene expression analysis
Plant hormone signaling
Plant pathogen resistance
Wheat genomics
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
27 May 2024
27 May 2024
Historique:
received:
04
03
2024
accepted:
20
05
2024
medline:
28
5
2024
pubmed:
28
5
2024
entrez:
27
5
2024
Statut:
epublish
Résumé
In this comprehensive genome-wide study, we identified and classified 83 Xylanase Inhibitor Protein (XIP) genes in wheat, grouped into five distinct categories, to enhance understanding of wheat's resistance to Fusarium head blight (FHB), a significant fungal threat to global wheat production. Our analysis reveals the unique distribution of XIP genes across wheat chromosomes, particularly at terminal regions, suggesting their role in the evolutionary expansion of the gene family. Several XIP genes lack signal peptides, indicating potential alternative secretion pathways that could be pivotal in plant defense against FHB. The study also uncovers the sequence homology between XIPs and chitinases, hinting at a functional diversification within the XIP gene family. Additionally, the research explores the association of XIP genes with plant immune mechanisms, particularly their linkage with plant hormone signaling pathways like abscisic acid and jasmonic acid. XIP-7A3, in particular, demonstrates a significant increase in expression upon FHB infection, highlighting its potential as a key candidate gene for enhancing wheat's resistance to this disease. This research not only enriches our understanding of the XIP gene family in wheat but also provides a foundation for future investigations into their role in developing FHB-resistant wheat cultivars. The findings offer significant implications for wheat genomics and breeding, contributing to the development of more resilient crops against fungal diseases.
Identifiants
pubmed: 38802731
doi: 10.1186/s12870-024-05176-4
pii: 10.1186/s12870-024-05176-4
doi:
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
462Informations de copyright
© 2024. The Author(s).
Références
Yi X, Cheng J, Jiang Z, Hu W, Bie T, Gao D, et al. Genetic analysis of Fusarium head blight resistance in CIMMYT bread wheat line C615 using traditional and conditional QTL mapping. Front Plant Sci. 2018;9:573.
pubmed: 29780395
pmcid: 5946024
doi: 10.3389/fpls.2018.00573
Shah L, Ali A, Yahya M, Zhu Y, Wang S, Si H, et al. Integrated control of Fusarium head blight and deoxynivalenol mycotoxin in wheat. Plant Pathol. 2018;67:532–48.
doi: 10.1111/ppa.12785
Semagn K, Henriquez MA, Iqbal M, Brûlé-Babel AL, Strenzke K, Ciechanowska I, et al. Identification of Fusarium head blight sources of resistance and associated QTLs in historical and modern Canadian spring wheat. Front Plant Sci. 2023;14:1190358.
pubmed: 37680355
pmcid: 10482112
doi: 10.3389/fpls.2023.1190358
Moonjely S, Ebert M, Paton-Glassbrook D, Noel ZA, Roze L, Shay R, et al. Update on the state of research to manage Fusarium head blight. Fungal Genet Biol. 2023;:103829.
Castro Aviles A, Alan Harrison S, Joseph Arceneaux K, Brown-Guidera G, Esten Mason R, Baisakh N. Identification of QTLs for resistance to Fusarium head blight using a doubled haploid population derived from southeastern united states soft red winter wheat varieties AGS 2060 and AGS 2035. Genes. 2020;11:699.
pubmed: 32630440
pmcid: 7349885
doi: 10.3390/genes11060699
The International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, Stein N, Feuillet C, Keller B, et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. 2018;361:eaar7191.
Zhu T, Wang L, Rimbert H, Rodriguez JC, Deal KR, De Oliveira R, et al. Optical maps refine the bread wheat Triticum aestivum cv Chinese Spring genome assembly. Plant J. 2021;107:303–14.
pubmed: 33893684
pmcid: 8360199
doi: 10.1111/tpj.15289
Carpita NC. Strcture and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:445–76.
pubmed: 15012297
doi: 10.1146/annurev.arplant.47.1.445
Chen C, Guo Q, He Q, Tian Z, Hao W, Shan X, et al. Comparative transcriptomic analysis of wheat cultivars differing in their resistance to Fusarium head blight infection during grain-filling stages reveals unique defense mechanisms at play. BMC Plant Biol. 2023;23:433.
pubmed: 37715120
pmcid: 10504723
doi: 10.1186/s12870-023-04451-0
Dong X, Meinhardt SW, Schwarz PB. Isolation and characterization of two endoxylanases from Fusarium graminearum. J Agric Food Chem. 2012;60:2538–45.
pubmed: 22313372
doi: 10.1021/jf203407p
Kulkarni N, Shendye A, Rao M. Molecular and biotechnological aspects of xylanases. FEMS Microbiol Rev. 1999;23:411–56.
pubmed: 10422261
doi: 10.1111/j.1574-6976.1999.tb00407.x
Prade RA. Xylanases: from biology to biotechnology. Biotechnol Genet Eng Rev. 1996;13:101–32.
pubmed: 8948110
doi: 10.1080/02648725.1996.10647925
Tundo S, Mandalà G, Sella L, Favaron F, Bedre R, Kalunke RM. Xylanase Inhibitors: defense players in plant immunity with implications in agro-Industrial processing. Int J Mol Sci. 2022;23:14994.
pubmed: 36499321
pmcid: 9739030
doi: 10.3390/ijms232314994
Fierens E, Rombouts S, Gebruers K, Goesaert H, Brijs K, Beaugrand J, et al. TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Biochem J. 2007;403:583–91.
pubmed: 17269932
pmcid: 1876379
doi: 10.1042/BJ20061291
Debyser W, Derdelinckx G, Delcour JA. Arabinoxylan solubilization and inhibition of the Barley malt xylanolytic system by wheat during mashing with wheat wholemeal adjunct: evidence for a new class of enzyme inhibitors in wheat. J Am Chem Soc. 1997;55:153–6.
Mclauchlan WR, Garcia-Conesa MT, Williamson G, Roza M, Ravestein P, Maat J. A novel class of protein from wheat which inhibits xylanases. Biochem J. 1999;338:441–6.
pubmed: 10024521
pmcid: 1220071
doi: 10.1042/bj3380441
Cao J, Lv Y, Hou Z, Li X, Ding L. Expansion and evolution of thaumatin-like protein (TLP) gene family in six plants. Plant Growth Regul. 2016;79:299–307.
doi: 10.1007/s10725-015-0134-y
Liu Y, Han N, Wang S, Chen C, Lu J, Riaz MW, et al. Genome-wide identification of Triticum aestivum xylanase inhibitor gene family and inhibitory effects of XI-2 subfamily proteins on Fusarium graminearum GH11 xylanase. Front Plant Sci. 2021;12:665501.
pubmed: 34381472
pmcid: 8350787
doi: 10.3389/fpls.2021.665501
Moscetti I, Tundo S, Janni M, Sella L, Gazzetti K, Tauzin A, et al. Constitutive expression of the xylanase inhibitor TAXI-III delays Fusarium head blight symptoms in durum wheat transgenic plants. Mol Plant Microbe Interact. 2013;26:1464–72.
pubmed: 23945000
doi: 10.1094/MPMI-04-13-0121-R
Tundo S, Kalunke R, Janni M, Volpi C, Lionetti V, Bellincampi D, et al. Pyramiding PvPGIP2 and TAXI-III but not PvPGIP2 and PMEI enhances resistance against Fusarium graminearum. Mol Plant Microbe Interact. 2016;29:629–39.
pubmed: 27366923
doi: 10.1094/MPMI-05-16-0089-R
Hou C, Lv T, Zhan Y, Peng Y, Huang Y, Jiang D, et al. Overexpression of the RIXI xylanase inhibitor improves disease resistance to the fungal pathogen, Magnaporthe oryzae, in rice. Plant Cell Tiss Organ Cult. 2015;120:167–77.
doi: 10.1007/s11240-014-0590-5
Sun R-J, Xu Y, Hou C-X, Zhan Y-H, Liu M-Q, Weng X-Y. Expression and characteristics of rice xylanase inhibitor OsXIP, a member of a new class of antifungal proteins. Biologia Plant. 2018;62:569–78.
doi: 10.1007/s10535-018-0787-2
Hou C-X, Zhan Y-H, Jiang D-A, Weng X-Y. Functional characterization of a new pathogen induced xylanase inhibitor (RIXI) from rice. Eur J Plant Pathol. 2014;138:405–14.
doi: 10.1007/s10658-013-0342-0
Lin P, Wong JH, Ng TB, Ho VSM, Xia L. A sorghum xylanase inhibitor-like protein with highly potent antifungal, antitumor and HIV-1 reverse transcriptase inhibitory activities. Food Chem. 2013;141:2916–22.
pubmed: 23871041
pmcid: 7115760
doi: 10.1016/j.foodchem.2013.04.013
Beaugrand J, Gebruers K, Ververken C, Fierens E, Croes E, Goddeeris B, et al. Antibodies against wheat xylanase inhibitors as tools for the selective identification of their homologues in other cereals. J Cereal Sci. 2006;44:59–67.
doi: 10.1016/j.jcs.2006.02.003
Croes E, Gebruers K, Carpentier S, Swennen R, Robben J, Laukens K, et al. A quantitative portrait of three xylanase inhibiting protein families in different wheat cultivars using 2D-DIGE and multivariate statistical tools. J Proteomics. 2009;72:484–500.
pubmed: 19245861
doi: 10.1016/j.jprot.2009.02.003
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47:D427-32.
pubmed: 30357350
doi: 10.1093/nar/gky995
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13:1194–202.
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, et al. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 2012;40:W597-603.
pubmed: 22661580
pmcid: 3394269
doi: 10.1093/nar/gks400
Yu C-S, Chen Y-C, Lu C-H, Hwang J-K. Prediction of protein subcellular localization. Proteins. 2006;64:643–51.
pubmed: 16752418
doi: 10.1002/prot.21018
Tamura K, Stecher G, Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022–7.
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34 Web Server:W369–73.
Schweiger W, Steiner B, Vautrin S, Nussbaumer T, Siegwart G, Zamini M, et al. Suppressed recombination and unique candidate genes in the divergent haplotype encoding Fhb1, a major Fusarium head blight resistance locus in wheat. Theor Appl Genet. 2016;129:1607–23.
pubmed: 27174222
pmcid: 4943984
doi: 10.1007/s00122-016-2727-x
Zhang S, Yu C, Liu X, Lai S, Wang W, Sun B, et al. Screening of scab-resistant wheat germplasms and distribution of Fhb1 gene. Acta Agriculturae Jiangxi. 2021;33:9–16.
Hu P, Ren Y, Xu J, Luo W, Wang M, Song P, et al. Identification of acyl-CoA-binding protein gene in Triticeae species reveals that TaACBP4A-1 and TaACBP4A-2 positively regulate powdery mildew resistance in wheat. Int J Biol Macromol. 2023;246:125526.
pubmed: 37379955
doi: 10.1016/j.ijbiomac.2023.125526
Borrill P, Ramirez-Gonzalez R, Uauy C. expVIP: a customizable RNA-seq data analysis and visualization platform. Plant Physiol. 2016;170:2172–86.
pubmed: 26869702
pmcid: 4825114
doi: 10.1104/pp.15.01667
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, et al. The transcriptional landscape of polyploid wheat. Science. 2018;361:eaar6089.
pubmed: 30115782
doi: 10.1126/science.aar6089
Steiner B, Buerstmayr M, Wagner C, Danler A, Eshonkulov B, Ehn M, et al. Fine-mapping of the Fusarium head blight resistance QTL Qfhs.ifa-5A identifies two resistance QTL associated with anther extrusion. Theor Appl Genet. 2019;132:2039–53.
Dalman MR, Deeter A, Nimishakavi G, Duan Z-H. Fold change and p-value cutoffs significantly alter microarray interpretations. BMC Bioinformatics. 2012;13:S11.
pubmed: 22536862
pmcid: 3305783
doi: 10.1186/1471-2105-13-S2-S11
Fei Y, Feng Z, Wu K, Luo Y, Yu L, Zhang Y, et al. MicroRNA expression profiling of caudal fin cell of C. auratus gibelio upon cyprinid herpesvirus 2 infection. Dev Comp Immunol. 2020;107:103637.
pubmed: 32035081
doi: 10.1016/j.dci.2020.103637
Deshmukh R, Singh A, Jain N, Anand S, Gacche R, Singh A, et al. Identification of candidate genes for grain number in rice (Oryza sativa L.). Funct Integr Genomics. 2010;10:339–47.
pubmed: 20376514
doi: 10.1007/s10142-010-0167-2
Kadam S, Singh K, Shukla S, Goel S, Vikram P, Pawar V, et al. Genomic associations for drought tolerance on the short arm of wheat chromosome 4B. Funct Integr Genomics. 2012;12:447–64.
pubmed: 22476619
doi: 10.1007/s10142-012-0276-1
Sonah H, Chavan S, Katara J, Chaudhary J, Kadam S, Patil G, et al. Genome-wide identification and characterization of Xylanase Inhibitor Protein (XIP) genes in cereals. Ind Jrnl Gen Plnt Bree. 2016;76:159.
doi: 10.5958/0975-6906.2016.00036.5
Wan J, He M, Hou Q, Zou L, Yang Y, Wei Y, et al. Cell wall associated immunity in plants. Stress Biol. 2021;1:3.
pubmed: 37676546
pmcid: 10429498
doi: 10.1007/s44154-021-00003-4
Sueldo DJ, Godson A, Kaschani F, Krahn D, Kessenbrock T, Buscaill P, et al. Activity-based proteomics uncovers suppressed hydrolases and a neo -functionalised antibacterial enzyme at the plant–pathogen interface. New Phytol. 2024;241:394–408.
pubmed: 36866975
doi: 10.1111/nph.18857
Abubakar YS, Sadiq IZ, Aarti A, Wang Z, Zheng W. Interplay of transport vesicles during plant-fungal pathogen interaction. Stress Biol. 2023;3:35.
pubmed: 37676627
pmcid: 10442309
doi: 10.1007/s44154-023-00114-0
Owji H, Nezafat N, Negahdaripour M, Hajiebrahimi A, Ghasemi Y. A comprehensive review of signal peptides: Structure, roles, and applications. Eur J Cell Biol. 2018;97:422–41.
pubmed: 29958716
doi: 10.1016/j.ejcb.2018.06.003
Wang X, Chung KP, Lin W, Jiang L. Protein secretion in plants: conventional and unconventional pathways and new techniques. J Exp Bot. 2018;69:21–37.
doi: 10.1093/jxb/erx262
Ding Y, Robinson DG, Jiang L. Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol. 2014;29:107–15.
pubmed: 24949560
doi: 10.1016/j.ceb.2014.05.008
Zhang M, Liu L, Lin X, Wang Y, Li Y, Guo Q, et al. A translocation pathway for vesicle-mediated unconventional protein secretion. Cell. 2020;181:637-652.e15.
pubmed: 32272059
doi: 10.1016/j.cell.2020.03.031
Rabouille C. Pathways of unconventional protein secretion. Trends Cell Biol. 2017;27:230–40.
pubmed: 27989656
doi: 10.1016/j.tcb.2016.11.007
Heidari P, Puresmaeli F, Mora-Poblete F. Genome-wide identification and molecular evolution of the Magnesium Transporter (MGT) gene family in Citrullus lanatus and Cucumis sativus. Agronomy. 2022;12:2253.
doi: 10.3390/agronomy12102253
Grzybowska EA. Human intronless genes: Functional groups, associated diseases, evolution, and mRNA processing in absence of splicing. Biochem Biophys Res Commun. 2012;424:1–6.
pubmed: 22732409
doi: 10.1016/j.bbrc.2012.06.092
Panchy N, Lehti-Shiu M, Shiu S-H. Evolution of gene duplication in plants. Plant Physiol. 2016;171:2294–316.
pubmed: 27288366
pmcid: 4972278
doi: 10.1104/pp.16.00523
Teli B, Purohit J, Rashid MdM, Jailani AAK, Chattopadhyay A. Omics insight on Fusarium head blight of wheat for translational research perspective. Curr Genomics. 2020;21:411–28.
pubmed: 33093804
pmcid: 7536796
doi: 10.2174/1389202921999200620222631
Cai H, Liu Y, Guo C. Contribution of plant–bacteria interactions to horizontal gene transfer in plants. Biotechnol Biotechnol Equip. 2021;35:1587–92.
doi: 10.1080/13102818.2021.1985612
Yi G, Sze S-H, Thon MR. Identifying clusters of functionally related genes in genomes. Bioinformatics. 2007;23:1053–60.
pubmed: 17237058
doi: 10.1093/bioinformatics/btl673
Dean RA. Fungal gene clusters. Nat Biotechnol. 2007;25:67–67.
pubmed: 17211403
doi: 10.1038/nbt0107-67
Flatman R, McLAUCHLAN RW, Juge N, Furniss C, Berrin J-G, Hughes RK, et al. Interactions defining the specificity between fungal xylanases and the xylanase-inhibiting protein XIP-I from wheat. Biochem J. 2002;365:773–81.
pubmed: 11955286
pmcid: 1222710
doi: 10.1042/bj20020168
Channamallikarjuna V, Sonah H, Prasad M, Rao GJN, Chand S, Upreti HC, et al. Identification of major quantitative trait loci qSBR11-1 for sheath blight resistance in rice. Mol Breeding. 2010;25:155–66.
doi: 10.1007/s11032-009-9316-5
Cui G, Hou J, Tong L, Xu Z. Light responsive elements and binding proteins of plant genes. Plant Physiol. 2010;46:991–1000.
Jing Y, Lin R. Transcriptional regulatory network of the light signaling pathways. New Phytol. 2020;227:683–97.
pubmed: 32289880
doi: 10.1111/nph.16602
Li T, Lian H, Li H, Xu Y, Zhang H. HY5 regulates light-responsive transcription of microRNA163 to promote primary root elongation in Arabidopsis seedlings. J Integr Plant Biol. 2021;63:1437–50.
pubmed: 33860639
doi: 10.1111/jipb.13099
Brookbank BP, Patel J, Gazzarrini S, Nambara E. Role of basal ABA in plant growth and development. Genes. 2021;12:1936.
pubmed: 34946886
pmcid: 8700873
doi: 10.3390/genes12121936
Hoheneder F, Steidele CE, Messerer M, Mayer K, Köhler N, Wurmser C, et al. Barley shows reduced Fusarium head blight under drought and modular expression of differential expressed genes under combined stress. J Exp Bot. 2023;74:6820–35.
pubmed: 37668551
doi: 10.1093/jxb/erad348
Chen K, Li G, Bressan RA, Song C, Zhu J, Zhao Y. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020;62:25–54.
pubmed: 31850654
doi: 10.1111/jipb.12899
Liu Z, Hou S, Rodrigues O, Wang P, Luo D, Munemasa S, et al. Phytocytokine signalling reopens stomata in plant immunity and water loss. Nature. 2022;605:332–9.
pubmed: 35508659
pmcid: 9710542
doi: 10.1038/s41586-022-04684-3
Melotto M, Underwood W, He SY. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol. 2008;46:101–22.
pubmed: 18422426
pmcid: 2613263
doi: 10.1146/annurev.phyto.121107.104959
Cao FY, Yoshioka K, Desveaux D. The roles of ABA in plant–pathogen interactions. J Plant Res. 2011;124:489–99.
pubmed: 21380629
doi: 10.1007/s10265-011-0409-y
Cheng H-Y, Wang Y, Tao X, Fan Y-F, Dai Y, Yang H, et al. Genomic profiling of exogenous abscisic acid-responsive microRNAs in tomato (Solanum lycopersicum). BMC Genom. 2016;17:423.
doi: 10.1186/s12864-016-2591-8
Li G, Yen Y. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Sci. 2008;48:1888–96.
doi: 10.2135/cropsci2008.02.0097
Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, et al. Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS One. 2011;6:e19008.
pubmed: 21533105
pmcid: 3080397
doi: 10.1371/journal.pone.0019008
Hao Y, Pan Y, Chen W, Rashid MAR, Li M, Che N, et al. Contribution of duplicated Nucleotide-binding Leucine-Rich Repeat (NLR) genes to wheat disease resistance. Plants. 2023;12:2794.
pubmed: 37570947
pmcid: 10420896
doi: 10.3390/plants12152794
Levy AA, Feldman M. Evolution and origin of bread wheat. Plant Cell. 2022;34:2549–67.
pubmed: 35512194
pmcid: 9252504
doi: 10.1093/plcell/koac130
Osawa S, Jukes TH, Watanabe K. Recent evidence for evolution of the genetic code. Microbiol Rev. 1992;56:229–64.
pubmed: 1579111
pmcid: 372862
doi: 10.1128/mr.56.1.229-264.1992
Kimura M. The neutral theory of molecular evolution: a review of recent evidence. Jpn J Genet. 1991;66:367–86.
pubmed: 1954033
doi: 10.1266/jjg.66.367
Vaghela B, Vashi R, Rajput K, Joshi R. Plant chitinases and their role in plant defense: a comprehensive review. Enzyme Microb Technol. 2022;159:110055.
pubmed: 35537378
doi: 10.1016/j.enzmictec.2022.110055
Oldach KH, Becker D, Lörz H. Heterologous expression of genes mediating enhanced fungal resistance in transgenic wheat. Mol Plant Microbe Interact. 2001;14:832–8.
pubmed: 11437256
doi: 10.1094/MPMI.2001.14.7.832
Hawkins LK, Mylroie JE, Oliveira DA, Smith JS, Ozkan S, Windham GL, et al. Characterization of the Maize chitinase genes and their effect on Aspergillus flavus and Aflatoxin accumulation resistance. PLoS One. 2015;10:e0126185.
pubmed: 26090679
pmcid: 4475072
doi: 10.1371/journal.pone.0126185
Ye W, Munemasa S, Shinya T, Wu W, Ma T, Lu J, et al. Stomatal immunity against fungal invasion comprises not only chitin-induced stomatal closure but also chitosan-induced guard cell death. Proc Natl Acad Sci USA. 2020;117:20932–42.
pubmed: 32778594
pmcid: 7456093
doi: 10.1073/pnas.1922319117
Ghasemi S, Ahmadian G, Sadeghi M, Zeigler DR, Rahimian H, Ghandili S, et al. First report of a bifunctional chitinase/lysozyme produced by Bacillus pumilus SG2. Enzyme Microb Technol. 2011;48:225–31.
pubmed: 22112904
doi: 10.1016/j.enzmictec.2010.11.001
Chen W, Jiang X, Yang Q. Glycoside hydrolase family 18 chitinases: The known and the unknown. Biotechnol Adv. 2020;43:107553.
pubmed: 32439576
doi: 10.1016/j.biotechadv.2020.107553
Yu J-B, Bai G-H, Zhou W-C, Dong Y-H, Kolb FL. Quantitative trait loci for Fusarium head blight resistance in a recombinant inbred population of Wangshuibai/Wheaton. Phytopathology. 2008;98:87–94.
pubmed: 18943242
doi: 10.1094/PHYTO-98-1-0087
Igawa T, Tokai T, Kudo T, Yamaguchi I, Kimura M. A wheat xylanase inhibitor gene, Xip-I, but Not Taxi-I, is significantly induced by biotic and abiotic signals that trigger plant defense. Biosci Biotechnol Biochem. 2005;69:1058–63.
pubmed: 15914935
doi: 10.1271/bbb.69.1058
Gan Y, Zhou Z, An L, Bao S, Forde BG. A comparison between northern blotting and quantitative real-time PCR as a means of detecting the nutritional regulation of genes expressed in roots of Arabidopsis thaliana. Agr Sci China. 2011;10:335–42.
doi: 10.1016/S1671-2927(11)60012-6
VanGuilder HD, Vrana KE, Freeman WM. Twenty-five years of quantitative PCR for gene expression analysis. BioTechniques. 2008;44:619–26.
pubmed: 18474036
doi: 10.2144/000112776