Silicon amendment induces synergistic plant defense mechanism against pink stem borer (Sesamia inferens Walker.) in finger millet (Eleusine coracana Gaertn.).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
06 03 2020
06 03 2020
Historique:
received:
03
11
2019
accepted:
19
02
2020
entrez:
8
3
2020
pubmed:
8
3
2020
medline:
24
11
2020
Statut:
epublish
Résumé
Silicon (Si) uptake and accumulation in plants can mitigate various biotic stresses through enhanced plant resistance against wide range of herbivores. But the role of silicon in defense molecular mechanism still remains to be elucidated in finger millet. In the present study, we identified three silicon transporter genes viz. EcLsi1, EcLsi2, and EcLsi6 involved in silicon uptake mechanism. In addition, the study also identified and characterized ten different Si transporters genes from finger millet through transcriptome assembly. The phylogenetic study revealed that EcLsi1 and EcLsi6 are homologs while EcLsi2 and EcLsi3 form another pair of homologs. EcLsi1 and EcLsi6 belong to family of NIP2s (Nod26-like major intrinsic protein), bona fide silicon transporters, whereas EcLsi2 and EcLsi3, an efflux Si transporter, belong to an uncharacterized anion transporter family having a significant identity with putative arsB transporter proteins. Further, the phylogenetic and topology analysis suggest that EcLsi1 and EcLsi2 co-evolved during evolution while, EcLsi2 and EcLsi3 are evolved from either EcLsi1 and/or EcLsi6 by fusion or duplication event. Moreover, these silicon transporters are predicted to be localized in plasma membrane, but their structural differences indicate that they might have differences in their silicon uptake ability. Silicon amendment induces the synergistic defense mechanism by significantly increasing the transcript level of silicon transporter genes (EcLsi1, EcLsi2 and EcLsi6) as well as defense hormone regulating genes (EcSAM, EcPAL and EcLOX) at 72 hpi (hours of post infestation) in both stem and roots compared to non-silicon treated plants against pink stem borer in finger millet plants. This study will help to understand the molecular defense mechanism for developing strategies for insect pest management.
Identifiants
pubmed: 32144322
doi: 10.1038/s41598-020-61182-0
pii: 10.1038/s41598-020-61182-0
pmc: PMC7060215
doi:
Substances chimiques
Plant Proteins
0
Silicon
Z4152N8IUI
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4229Références
Rudin, B., Shashidhar, H. E., Kulkarni, R. S. & Hittalmani, S. Genetic diversity assessment of finger millet, (Eleusine coracana (L) Gaertn), germplasm through RAPD analysis. PGR Newslett 138, 50–54 (2004).
Reddy, V. G., Upadhyaya, H. D., Gowda, C. L. L. & Singh, S. Characterization of Eastern African finger millet germplasms for qualitative characters at ICRISAT. J. SAT Agricultural Res. 7, 1–9 (2009).
Gahukar, R. T. Potential of minor food crops and wild plants for nutritional security in the developing world. J. Agriculture and Food Information 15, 342–352 (2014).
doi: 10.1080/10496505.2014.952429
Kumar, A., Tomar, V., Kaur, A., Kumar, V. & Gupta, K. Millets: a solution to agrarian and nutritional challenges. Agric. Food Secur. 7, 31 (2018).
doi: 10.1186/s40066-018-0183-3
Sasmal, A., Mohapatra, A. K. B. & Pradhan, K. C. Screening of finger millet genotypes against pink stem borer (Sesamia inferens Walker, Noctuidae, Lepidoptera). J. Entomology and Zoology Studies 6, 796–799 (2018).
Li, C. X., Cheng, X. & Dai, S. M. Distribution and insecticide resistance of pink stem borer, Sesamia inferens (Lepidoptera: Noctuidae), in Taiwan. Formosan Entomol. 31, 39–50 (2011).
Gahukar, R. T. & Reddy, G. V. P. Management of Economically Important Insect Pests of Millet. J. Integrated Pest Management 10, 28 (2019).
doi: 10.1093/jipm/pmz026
Ma, J. F. & Takahashi, E. Soil, fertilizer and plant silicon research in Japan, Elsevier Science, Amsterdam, The Netherlands, 294 (2002).
Ma, J. F. & Yamaji, N. Silicon uptake and accumulation in higher plants. Trends in Plant Sci. 11, 392–397 (2006).
doi: 10.1016/j.tplants.2006.06.007
Epstein, E. Silicon. Annual Review of Plant Physiology and Plant Molecular Biol. 50, 641–664 (1999).
doi: 10.1146/annurev.arplant.50.1.641
Debona, D., Rodrigues, F. A. & Datnoff, L. E. Silicon’s role in abiotic and biotic plant stresses. Ann. Rev. Phytopath. 55, 85–107 (2017).
doi: 10.1146/annurev-phyto-080516-035312
Hou, M. & Han, Y. Silicon-mediated rice plant resistance to the Asiatic rice borer (Lepidoptera: Crambidae): Effects of silicon amendment and rice varietal resistance. J. Econ. Entomol. 103, 1412–1419 (2010).
doi: 10.1603/EC09341
Fauteux, F., Rémus-Borel, W., Menzies, J. G. & Bélanger, R. R. Silicon and plant disease resistance against pathogenic fungi. FEMS MicrobiolLett. 249, 1–6 (2005).
doi: 10.1016/j.femsle.2005.06.034
Ali, J. G. & Agrawal, A. A. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293–302 (2012).
doi: 10.1016/j.tplants.2012.02.006
De Vos, M. et al. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact. 18, 923–937 (2005).
doi: 10.1094/MPMI-18-0923
Kessler, A. & Baldwin, I. T. Plant responses to insect herbivory: The emerging molecular analysis. Ann. Rev Plant Biol. 53, 299–328 (2002).
doi: 10.1146/annurev.arplant.53.100301.135207
Kindt, F., Joosten, N. N., Peters, D. & Tjallingii, W. F. Characterization of the feeding behavior of western flower thrips in terms of electrical penetration graph (EPG) waveforms. Jour Insect Physiol. 49, 183–191 (2003).
doi: 10.1016/S0022-1910(02)00255-X
Moran, P. J. & Thompson, G. A. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125, 1074–1085 (2001).
doi: 10.1104/pp.125.2.1074
pubmed: 64906
pmcid: 64906
Liu, J. et al. Silicon supplementation alters the composition of herbivore induced plant volatiles and enhances attraction of parasitoids to infested rice plants. Front Plant Sci. 8(725), 1265 (2017).
doi: 10.3389/fpls.2017.01265
pubmed: 5515826
pmcid: 5515826
Reynolds, O. L., Keeping, M. G. & Meyer, J. H. Silicon-augmented resistance of plants to herbivorous insects: A review. Ann. Appl.Biol. 155, 171–186 (2009).
doi: 10.1111/j.1744-7348.2009.00348.x
Hartley, S. E. & DeGabriel, J. L. The ecology of herbivore-induced silicon defenses in grasses. Functional Ecol. 30, 1311–1322 (2016).
doi: 10.1111/1365-2435.12706
Pappas, M. L. et al. Induced plant defences in biological control of arthropod pests: A double-edged sword. Pest Manag Sci. 73, 1780–1788 (2017).
doi: 10.1002/ps.4587
pubmed: 5575458
pmcid: 5575458
Grégoire, C. et al. Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. Plant J. 72, 320–330 (2012).
doi: 10.1111/j.1365-313X.2012.05082.x
Wang, H. S. et al. Identification of two cucumber putative silicon transporter genes in Cucumis sativus. J. Plant Growth Regul. 34, 332–338 (2015).
doi: 10.1007/s00344-014-9466-5
Mitani, N. et al. Isolation and functional characterization of an influx silicon transporter in two pumpkin cultivars contrasting in silicon accumulation. Plant J. 66, 231–240 (2011).
doi: 10.1111/j.1365-313X.2011.04483.x
Ma., J. F. An efflux transporter of silicon in rice. Nature 448, 209–12 (2007).
doi: 10.1038/nature05964
Mitani, N., Chiba, Y., Yamaji, N. & Ma, J. F. Identification and characterization of maize and barley Lsi2-like silicon efflux transporters reveals a distinct silicon uptake system from that in rice. Plant Cell. 21, 2133–2142 (2009).
doi: 10.1105/tpc.109.067884
pubmed: 2729598
pmcid: 2729598
Ma, J. F., Yamaji, N. & Mitani-Ueno, N. Transport of silicon from roots to panicles in plants. ProcJapanAcadSer B Phys. Biol. Sci. 87, 377–385 (2011).
doi: 10.2183/pjab.87.377
Ma, J. F. Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr. 50, 11–18 (2004).
doi: 10.1080/00380768.2004.10408447
Yang, L. et al. Silicon amendment is involved in the induction of plant defense responses to a phloem feeder. Scientific Reports. 7, 4232 (2017).
doi: 10.1038/s41598-017-04571-2
pubmed: 5484686
pmcid: 5484686
Sun, H. et al. Isolation and functional characterization of CsLsi1, a silicon transporter gene in Cucumissativus. Physiol Plantarum 159, 201–214 (2017).
doi: 10.1111/ppl.12515
Sun, H. et al. Isolation and functional characterization of CsLsi2, a cucumber silicon efflux transporter gene. Annals of Bot. 122, 641–648 (2018).
doi: 10.1093/aob/mcy103
Zellner, W., Lutz, L., Khandekar, S. & Leisner, S. Identification of NtNIP2; 1: an Lsi1 silicon transporter in Nicotiana tabacum. Jour Plant Nutrition. 42, 1028–1035 (2019).
doi: 10.1080/01904167.2019.1589500
Chiba, Y., Mitani, N., Yamaji, N. & Ma, J. F. HvLsi1 is a silicon influx transporter in barley. Plant Jour 57, 810–818 (2009).
doi: 10.1111/j.1365-313X.2008.03728.x
Mitani, N., Yamaji, N. & Ma, J. F. Identification of maize silicon influx transporters. Plant Cell Physiol. 50, 5–12 (2009).
doi: 10.1093/pcp/pcn110
pubmed: 18676379
pmcid: 18676379
Montpetit, J. et al. Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant MolBiol. 79, 35–46 (2012).
Deshmukh, R. K. et al. Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol. Biol. 83, 303–315 (2013).
doi: 10.1007/s11103-013-0087-3
pubmed: 23771580
pmcid: 23771580
Ma, J. F. & Yamaji, N. A cooperative system of silicon transport in plants. Trends in Plant Sci. 20, 435–442 (2015).
doi: 10.1016/j.tplants.2015.04.007
Zhu, Y. X., Gong, H. J. & Yin, J. L. Role of Silicon in Mediating Salt Tolerance in Plants: A Review. Plants 8, 147 (2019).
doi: 10.3390/plants8060147
Marron, A. O. et al. The evolution of silicon transport in eukaryotes. Molecular Biol.Evol. 33, 3226–3248 (2016).
doi: 10.1093/molbev/msw209
Wangkaew, B., Prom-u-thai, C. T., Jamjod, S., Rerkasem, B. & Pusadee, T. Silicon concentration and expression of silicon transport genes in two Thai rice Varieties. CMU J. Nat Sci. 18, 358–372 (2019).
Yamaji, N. & Ma, J. F. A Transporter at the node responsible for intervascular transfer of silicon in rice. The Plant Cell. 21, 2878–2883 (2009).
doi: 10.1105/tpc.109.069831
pubmed: 2768918
pmcid: 2768918
Ye, M. et al. Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc. Nati. Acad. Sci. 110, E3631–E3639 (2013).
doi: 10.1073/pnas.1305848110
Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann. Rev. Phytopathol. 43, 205–227 (2005).
doi: 10.1146/annurev.phyto.43.040204.135923
Wu, J. & Baldwin, I. T. New insights into plant responses to the attack from insect herbivores. Ann. Rev. Genetics. 44, 1–24 (2010).
doi: 10.1146/annurev-genet-102209-163500
Kahl, J. et al. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210, 336–342 (2000).
doi: 10.1007/PL00008142
Spoel, S. H. et al. NPR1 modulates cross-talk between salicylate and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell. 15, 760–786 (2003).
doi: 10.1105/tpc.009159
pubmed: 150028
pmcid: 150028
Bandong, J. P. & Litsinger, J. A. Rice crop stage susceptibility to the rice yellow stem borer Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae). Int. J. Pest Management. 51, 37–43 (2005).
doi: 10.1080/09670870400028276
Tripathy, S. & Rath, L. K. Silicon induced resistance expression in rice to Yellow stem borer. J. Entomology and Zoology Studies. 5, 12–15 (2017).
Ranganathan, S. et al. Effect of silicon sources on its deposition, chlorophyll content, and disease pest resistance in rice. Biol. Plantarum. 50, 713–716 (2006).
doi: 10.1007/s10535-006-0113-2
Chandramani, P., Rajendran, R., Sivasubramanian, P., Muthiah, C. & Chinniah, C. Organic source induced silica on leaf folder, stem borer and gall midge population and rice yield. J. Biopesticides 3, 423–427 (2010).
Hoagland, D. R. &Arnon, D. I. The water culture method for growing plant without soil. California Agri Exp. Sta Cir. No. 347 (University of California Berkley Press, CA, USA.) (1950).
Nikolic, M., Nikolic, N., Liang, Y., Kirkby, E. A. & Römheld, V. Germanium-68 as an adequate tracer for silicon transport in plants. Characterization of silicon uptake in different crop species. Plant Physiol. 143, 495–503 (2007).
Takahashi, E. & Hino, K. Silica uptake by plant with special reference to the forms of dissolved silica. Jap J. Soil Sci and Manure 49, 357–360 (1978).
Dai, W. M. Rapid determination of silicon content in rice. Rice Sci 12, 145–147 (2005).
Hittalmani, H. et al. Genome and transcriptome sequence of finger millet (Eleusine coracana (L.) Gaertn.) provides insights into drought tolerance and nutraceutical properties. BMC Genomics 18, 465 (2017).
doi: 10.1186/s12864-017-3850-z
pubmed: 5472924
pmcid: 5472924
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–20 (2014).
doi: 10.1093/bioinformatics/btu170
pubmed: 4103590
pmcid: 4103590
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotech. 29, 644–652 (2011).
doi: 10.1038/nbt.1883
Gasteiger, E, et al Protein Identification and Analysis Tools on the ExPASy Server. In: Walker J.M. (ed) The Proteomics Protocols Handbook. Humana Press, New York, USA, pp 571–607 (2005).
Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Stemberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols 10, 845–858 (2015).
doi: 10.1038/nprot.2015.053
pubmed: 5298202
pmcid: 5298202
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol and Evol. 33, 1870–1874 (2016).
doi: 10.1093/molbev/msw054
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408 (2001).
doi: 10.1006/meth.2001.1262
pubmed: 11846609
pmcid: 11846609