Abstract
Gossypium hirsutum L. represents the best cotton species for fiber production, thus computing the largest cultivated area worldwide. Meloidogyne incognita is a root-knot nematode (RKN) and one of the most important species of Meloidogyne genus, which has a wide host range, including cotton plants. Phytonematode infestations can only be partially controlled by conventional agricultural methods, therefore, more effective strategies to improve cotton resistance to M. incognita disease are highly desirable. The present study employed functional genomics to validate the involvement of two previously identified candidate genes, encoding dirigent protein 4—GhDIR4 and peroxiredoxin-2—GhPRXIIB, in cotton defense against M. incognita. Transgenic A. thaliana plant lines overexpressing GhDIR4 and GhPRXIIB genes were generated and displayed significantly improved resistance against M. incognita infection in terms of female nematode abundance in the roots when compared to wild-type control plants. For our best target-gene GhDIR4, an in-silico functional analysis, including multiple sequence alignment, phylogenetic relationship, and search for specific protein motifs unveiled potential orthologs in other relevant crop plants, including monocots and dicots. Our findings provide valuable information for further understanding the roles of GhDIR and GhPRXIIB genes in cotton defense response against RKN nematode.
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References
Alvarez A, Montesano M, Schmelz E, Ponce de León I (2016) Activation of shikimate, phenylpropanoid, oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Front Plant Sci 7:328. https://doi.org/10.3389/fpls.2016.00328
Barbosa AEAD, da Rocha RF, de Lima e Souza DS, et al (2009) Differentially expressed genes in cotton plant genotypes infected with Meloidogyne incognita. Plant Sci 177:492–497. https://doi.org/10.1016/j.plantsci.2009.07.013
Borong L, Xue Q, Jinling L, Kan Z (2020) Role of protein glycosylation in host-pathogen interaction. Cell 9:1–24. https://doi.org/10.3390/cells9041022
Brasileiro, ACM; Carneiro VTC (2015) Manual de transformação genética de plantas, 2° edition. Embrapa, Brasília-DF
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313X.1998.00343.x
Di Tommaso P, Moretti S, Xenarios I et al (2011) T-Coffee: A web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:13–17. https://doi.org/10.1093/nar/gkr
Dvořák P, Krasylenko Y, Zeiner A et al (2021) Signaling toward reactive oxygen species-scavenging enzymes in plants. Front Plant Sci 11:618835. https://doi.org/10.3389/fpls.2020.618835
Hasanuzzaman M, Bhuyan MHMB, Parvin K et al (2020) Regulation of ROS metabolism in plants under environmental stress: a review of recent experimental evidence. Int J Mol Sci 21:1–44. https://doi.org/10.3390/ijms21228695
Hidalgo P, Garretón V, Berríos CG, Ojeda H, Jordana X, Holuigue L (2001) A nuclear casein kinase 2 activity is involved in early events of transcriptional activation induced by SA in Tobacco. Plant Physiol 125:396–405. https://doi.org/10.1104/pp.125.1.396
Hu TT, Pattyn P, Bakker EG et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–483. https://doi.org/10.1038/ng.807
Jans Y, Von Bloh W, Schaphoff S et al (2021) Global cotton production under climate change-implications for yield and water consumption. Hydrol Earth Syst Sci 25:2027–2044. https://doi.org/10.5194/hess-25-2027-2021
Jones JDG, Dang JL (2006) The plant immunity. Nature 444:323–329
Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant. Trends Plant Sci 7:193–195
Khan A, Li RJ, Sun JT et al (2018) Genome-wide analysis of dirigent gene family in pepper (Capsicum annuum L.) and characterization of CaDIR7 in biotic and abiotic stresses. Sci Rep 8:1–27. https://doi.org/10.1038/s41598-018-23761-0
Kiba A, Nishihara M, Tsukatani N et al (2005) A peroxiredoxin Q homolog from gentians is involved in both resistance against fungal disease and oxidative stress. Plant Cell Physiol 46:1007–1015. https://doi.org/10.1093/pcp/pci109
Kneeshaw S, Gelineau S, Tada Y et al (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162. https://doi.org/10.1016/j.molcel.2014.08.003
Kumar S, Stecher G, Li M et al (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lambertucci S, Orman KM, Das Gupta S et al (2019) Analysis of barley leaf epidermis and extrahaustorial proteomes during Powdery Mildew infection reveals that the PR5 thaumatin-Like protein TLP5 is required for susceptibility towards Blumeria graminis f. sp. hordei. Front Plant Sci 10:23. https://doi.org/10.3389/fpls.2019.01138
Li YB, Han LB, Wang HY et al (2016) The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiol 170:2392–2406. https://doi.org/10.1104/pp.15.01930
Li N, Zhao M, Liu T et al (2017) A novel soybean dirigent gene GmDIR22 contributes to promotion of lignan biosynthesis and enhances resistance to Phytophthora sojae. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01185
Liu Z, Wang X, Sun Z et al (2021) Evolution, expression and functional analysis of cultivated allotetraploid cotton DIR genes. BMC Plant Biol 21:1–16. https://doi.org/10.1186/s12870-021-02859-0
Macharia TN, Bellieny-Rabelo D, Moleleki LN (2020) Transcriptome profiling of potato (Solanum tuberosum L.) responses to root-knot nematode (Meloidogyne javanica) infestation during a compatible interaction. Microorganisms 8:1–17. https://doi.org/10.3390/microorganisms8091443
Malik WA, Wang X, Wang X et al (2020) Genome-wide expression analysis suggests glutaredoxin genes response to various stresses in cotton. Int J Biol Macromol 153:470–491. https://doi.org/10.1016/j.ijbiomac.2020.03.021
Nolte H, MacVicar TD, Tellkamp F, Krüger M (2018) Instant Clue: a software suite for interactive data visualization and analysis. Sci Rep 8(1):6–13. https://doi.org/10.1038/s41598-018-31154-6
Olsen JV, Blagoev B, Gnad F et al (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:635–648. https://doi.org/10.1016/j.cell.2006.09.026
Pawan K, Sameer K, Mychele DS, Rippy S, Richard FD, Robert L, Nichols PWC (2019) Transcriptome analysis of a nematode resistant and susceptible upland cotton line at two critical stages of Meloidogyne incognita infection and development. PLoS ONE 14:19. https://doi.org/10.1371/journal.pone.0221328
Peterson T (ed) (2013) Plant Transposable Elements, 1057th edn. Springer, New York
Podesta N, (2022) Cotton and Products Annual - BR2022–0030. USDA and Global Agricultural Information Network. Brasília, Brazil. Report link: chromeextension://efaidnbmnnnibpcajpcglclefindmkaj/https://apps.fas.usda.gov/newgainapi/api/Report/DownloadReportByFileName?fileName=Cotton%20and%20Products%20Annual_Brasilia_Brazil_BR2022-0030.pdf
Reboledo G, del Campo R, Alvarez A et al (2015) Physcomitrella patens activates defense responses against the pathogen colletotrichum gloeosporioides. Int J Mol Sci 16:22280–22298. https://doi.org/10.3390/ijms160922280
Santos IR, Rios TB, Maximiano MR et al (2021) Proteomic screening for the identification of proteins involved in resistance to Xanthomonas campestris pv. malvacearum in cotton. Physiol Mol Plant Pathol 113:101562. https://doi.org/10.1016/j.pmpp.2020.101562
Sheth K (2017) The leading cotton exporting countries in the world. In: World Atlas. https://www.worldatlas.com/articles/top-cotton-producing-countries-in-theworld.
Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108:451–457. https://doi.org/10.1104/pp.108.2.451
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Junqi Song XD (2013) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:1–9
Távora FTPK, Santos C, Maximiano MR et al (2019) Pan proteome of Xanthomonas campestris pv. campestris isolates contrasting in virulence. Proteomics 19:1–30. https://doi.org/10.1002/pmic.201900082
Távora FTPK, Bevitori R, Mello RN et al (2021) Shotgun proteomics coupled to transient-inducible gene silencing reveal rice susceptibility genes as new sources for blast disease resistance. J Proteomics 241:104223. https://doi.org/10.1016/j.jprot.2021
Taylor RAJ (2019) Nematodes and other worms. Chapter 7, In: Taylor’s Power Law. Academic Press, ISBN 9780128109878, pp 143–234
Terry AW, Kerry S, Monclova-Santana C, Jane KD (2020) The relationship between commercial cotton cultivars with varying Meloidogyne incognita resistance genes and yield. J Nematol 52:8
Udenwobele DI, Su RC, Good SV et al (2017) Myristoylation: An important protein modification in the immune response. Front Immunol 8:1–16
Untergasser A, Cutcutache I, Koressaar T et al (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:1–12
Vilela B, Pagès M, Riera M (2015) Emerging roles of protein kinase CK2 in abscisic acid signaling. Front Plant Sci 6:1–9
Wu Z, Yang Y, Huang G et al (2017) Cotton functional genomics reveals global insight into genome evolution and fiber development. J Genet Genomics 44:511–518
Yang Z, Qanmber G, Wang Z et al (2020) Gossypium genomics: trends, scope, and utilization for cotton improvement. Trends Plant Sci 25:488–500
Acknowledgements
This study was financed by Embrapa, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), INCT-PlantStress Biotech, and FAPDF.
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CS, LSTC, RFCL, PNM, LBDL and MELS performed the experiments. FTPKT performed statistical analysis and wrote the manuscript. MFGS supervised the work. AM conceived the idea, obtained the resources and was in charge of overall supervision and project administration. All authors read and approved the final manuscript.
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Additional file 1: Table S1.
List of primer pairs used in the study.
Additional file 2: Figure S1.
Molecular main steps involved in the construction of plasmid vector pK7WGF2 used in the study for gene overexpression.
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dos Santos, C., Carmo, L.S.T., Távora, F.T.P.K. et al. Overexpression of cotton genes GhDIR4 and GhPRXIIB in Arabidopsis thaliana improves plant resistance to root-knot nematode (Meloidogyne incognita) infection. 3 Biotech 12, 211 (2022). https://doi.org/10.1007/s13205-022-03282-4
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DOI: https://doi.org/10.1007/s13205-022-03282-4