Investigation of microRNA-mediated redox regulation in leaf growth regions during chiling stress tolerance of maize (Zea mays L.)

Yıl 2019, Cilt: 34 Sayı: 2, 172 - 183, 25.06.2019

Fatma Aydinoglu Burak Akgul

https://doi.org/10.7161/omuanajas.482710

Öz

Corn (Zea mays L.) is one of the temperate
climate crops, very sensitive to chilling stress and needs  relatively high temperature for optimum growth
and high yield. Chilling stress disrupts growth processes coupled with
disruption of redox homeostasis of the cell, leading to oxidative stress. It is
also known that the low amount of reactive oxygen species (ROS) released during
this period promote growth. From that view, the aim of this study was to
investigate the possible microRNA (miRNA) mediated regulation of ROS playing
signalling role in leaf growth response against the chilling stress of maize
seedlings. In this respect, ROS production was triggered by applying low night
temperature stress to maize hybrid seedlings named ADA313. The antioxidant
genes that play a major role in the redox regulation and the microRNAs
targeting them were determined by in silico analysis and the relationship
between them was validated at the transcriptional and enzymatic level. As a
result, the elongation rate of the fourth leaf was reduced by 19% by chilling
stress compared to control. miR528, which was predicted to target SOD 1a gene
was found meristem and stress specific. The expression of miR397, which was
predicted to target Laccase, was detected at maturity. Enzymatic activities of
catalase (CAT), superoxide dismutase (SOD), glutathione reductase (GR),
peroxidase (POX) and ascorbate peroxidase (APX) were found to differ between
the growth regions. In this study, the miRNA-mediated regulation of the
oxidative signaling pathway was shown for the first time in the leaf growth
zones of maize response to chilling stress.

Anahtar Kelimeler

Leaf growth, miRNA, Oxidative signaling, ROS, Zea mays

Mısır (Zea mays L.) bitkisinin üşüme stresine toleransı sırasında yaprak büyüme bölgelerinde mikroRNA aracılıklı redoks regülasyonunun incelenmesi

Öz

Ilıman iklim tahıllarından olan mısır
(Zea mays L.) bitkisi, üşüme stresine
oldukça duyarlıdır ve optimum büyüme ve yüksek verim için nispeten yüksek
sıcaklığa ihtiyaç duyar. Üşüme stresi, büyüme işlevlerini sekteye uğratmakla
birlikte hücrenin redoks homeostazisini bozarak oksidatif strese yol açar. Bu
sırada açığa çıkan reaktif oksijen türleri (ROS)’in ise düşük miktarlarda
büyümeyi teşvik ettikleri de bilinmektedir. Buradan yola çıkarak, bu çalışmada,
mısır fidelerinin üşüme stresine karşı yaprak büyüme cevabının oluşumunda
sinyal role sahip reaktif oksijen türlerinin microRNA (miRNA) genleri ile olası
regülasyonunun araştırılması amaçlanmıştır. 
Bu doğrultuda, ADA 313 adlı mısır hibridi fidelerine üşüme stresi
uygulanarak ROS üretimi tetiklenmiştir. 
Redoks regülasyonunda başlıca rol oynayan antioksidan genleri ve onları
hedef alan microRNA’lar in silico
analizlerle belirlenerek, aralarındaki ilişki transkripsiyonel ve enzimatik
seviyede gösterilmiştir. Sonuç
olarak, yaprak uzama oranı stres koşullarında kontrole göre %19 azalmıştır. SOD 1a
genini hedef aldığı tahmin edilen miR528’in stres ve meristem, miR397 ve
tahmini hedefi Lakkaz’ın olgunluk
spesifik olduğu saptanmıştır. Katalaz (CAT), süperoksit dismutaz (SOD),
glutatyon redüktaz (GR), peroksidaz (POX) ve askorbat peroksidaz (APX)
antioksidan enzimlerinin aktivitelerinin büyüme bölgeleri arasında farklılık
gösterdiği görülmüştür.  Bu çalışma ile
ilk defa, mısır bitkisinin üşüme stresine toleransı sırasında yaprak büyüme
cevabında oksidatif sinyalizasyonun miRNA genleriyle regülasyonu
gösterilmiştir.

Anahtar Kelimeler

miRNA, ROS, Oksidatif sinyalizasyon, Yaprak büyümesi, Mısır

Kaynakça

• Aebi, H.E., 1983. Catalase. In: Bergmeyer, H.U., Ed., Methods of Enzymatic Analysis, Verlag Chemie, Weinhem, 273- 286.
• Avramova, V., AbdElgawad H., Zhang, Z., Fotschki, B., Casadevall, R., Vergauwen L., Knapen, D., Taleisnik, E., Guisez, Y., Asard, H., Beemster, G.T., 2015. Drought induces distinct growth response, protection, and recovery mechanisms in the maize leaf growth zone. Plant Physiology, 169, 1382–1396.
• Banowetza, G.M., Dierksena, K.P., Azevedoa, M.D., Stout, R., 2004. ‘Microplate quantification of plant leaf superoxide dismutases. Analytical Biochemistry, 332, 314–320.
• Bartel, D.P., 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.
• Beemster, G.T.S., Fiorani, F., Inze, D., 2003. Cell cycle: The key to plant growth control?. Trends in Plant Science, 8, 154-158.
• Boudolf, V., Vlieghe, K., Beemster, G.T., Magyar, Z., Torres-Acosta, J.A., Maes, S., Van Der Schueren, E., Inze, D., De Veylder, L., 2004. The plantspecific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. The Plant Cell, 16, 2683–2692.
• Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 72, 248–254.
• Crevecoeur, M., Marcela, P., Greppin, H., Penell, C., 1997. Peroxidase activity in shoot apical meristem from Spinaci. Acta Histochemica, 99, 177-186.
• Chavez-Hernandez, E.C., Alejandri-Ramirez, N.D., Juarez-Gonzalez V. T., Dinkova, T. D., 2015. Maize miRNA and target regulation in response to hormone depletion and light exposure during somatic embryogenesis. Frontial Plant Science, 22;6: 555-569.
• Chance, B. , Maehly, A.C., 1995. Assay of catalases and peroxidases. Methods in Enzymology, 2, 764-775.
• Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V. R., Andersen, M.R., Lao, K.Q., Livak, K.J., Guegler, K.J., 2005. Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Research, 33 (20), e179.
• Choudhury, F.K., Rivero, R.M., Blumwald, E., Mittler, R., 2017. Reactive oxygen species, abiotic stress and stress combination. The Plant Journal, 90, 856–867.
• Chinnusamy, V., Zhu, J., Zhu, J., 2007. Cold stress regulation of gene expression in plants. TRENDS in Plant Science, 12, 10.
• Kumar, A., Sharmaa, K.K., Kumar, P., Ramchiaryb, N., 2015. Laccase isozymes from Ganoderma lucidum MDU-7: isolation, characterization, catalytic properties and differential role during oxidative stress. Journal of Molecular Catalysis B: Enzymatic 113, 68–75.
• Considine, M.J., Foyer, C.H., 2014. Redox regulation of plant development. Antioxid Redox Signal. 20;21(9):1305-26.
• Dai, X., Zhuang, Z., Zhao, P.X., 2018. psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res. 46, W49-W54.
• de Azevedo Neto, A.D., Prisco, J. T., Enéas-Filho J., de Abreu, C.E.B., Gomes-Filho, E., 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environmental and Experimental Botany, 56, 87–94.
• Eker, S., Ozturk, L., Yazici, A., Erenoglu, B., Romheld, V., Cakmak, I., 2006. Foliar-applied glyphosate substantially reduced uptake and transport of iron and manganese in sunflower (Helianthus annuus L.) plants. J Agric Food Chem. Dec 27;54(26):10019-25.
• Gupta, O.P., Meena, N.L., Sharma, I., Sharma P., 2014. Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Molecular Biology Reports, 41,4623–4629.
• Lichtenthaler, H.K., Buschmann, C., 2001. Current Protocols in Food Analytical Chemistry, F4.3.1-F4.3.8.
• Inze, D., Veylder, L., 2006. Cell Cycle Regulation in Plant Development. The Annual Review of Genetics, 40, 77–105.
• Jones-Rhoades, M.W., Bartel, D.P., 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Moleculer Cell, 14, 787–799.
• Kayıhan, D.S., Kayıhan, C., Çiftçi, Y.Ö., 2016. Excess boron responsive regulations of antioxidative mechanism at physio-biochemical and molecular levels in Arabidopsis thaliana. Plant Physiology and Biochemistry, 109:337-345.
• Khraiwesh, B., Zhu, J.K., Zhu, J., 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta., 1819(2):137-48.
• Lee, D.H., Lee, C.B., 2000. Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci., 16;159(1):75-85.
• Lee, S.J., Jeong, E.M., Ki, A.Y., Oh, K.S., Kwon, J., Jeong, J.H., Chung, N.J., 2016. Oxidative defense metabolites induced by salinity stress in roots of Salicornia herbacea. J Plant Physiol., 1(206): 133-142.
• Ma, C., Burd, S., Lers, A. 2015. miR408 is involved in abiotic stress responses in Arabidopsis. The Plant Journal, 84: 169–187.
• Mabuchi, K., Maki, H., Itaya, T., Suzuki, T., Nomoto, M., Sakaoka, S., Morikami, A., Higashiyama, T., Tada, Y., Busch, W., Tsukagoshi, H., 2018. MYB30 links ROS signaling, root cell elongation, and plant immune responses. Proc Natl Acad Sci U S A. 15;115(20): E4710-E4719.
• Li, L., Yi, H., Xue, M., Yi, M., 2017. miR398 and miR395 are involved in response to SO2 stress in Arabidopsis thaliana. Ecotoxicology. 26(9):1181-1187.
• Liu Q, Hu H, Zhu L, Li R, Feng Y, Zhang L, Yang Y, Liu X, Zhang H. (2015), Involvement of miR528 in the regulation of arsenite tolerance in rice (Oryza sativa L.). J Agric Food Chem. 14;63(40): 8849-8861.
• Menon, S.G., Goswami, P.C., 2007. A redox cycle within the cell cycle: ring in the old with the new. Oncogene. 22;26(8): 1101-1109.
• Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C., Weigel, D. 2003. Control of leaf morphogenesis by microRNAs. Nature, 425: 257–263.
• Pfaffl, M.W., 2001. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research, 29(9): e45.
• Quesada, M. A., Sfinchez-Roldfin, C., Heredia, A., Valpuesta, V., Bukovac, M.J., 1992. Peroxidase and IAA oxidase activities and peroxidase isoenzymes in the pericarp of seeded and seedless "Redhaven" peach fruit. Journal of Plant Growth Regulation, 11: 1-6.
• Rymen, B., Fiorani, F., Kartal, F., Vandepoele, K., Inze, D., Beemster, G. T. S., 2007. Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiology, 143 (3), 1429-1438.
• Scandalios, J.G., 2005. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research, 38: 995-1014.
• Song, Q.X., Liu, Y.F., Hu, X.Y., Zhang, W.K., Ma, B., Chen, S.Y., Zhang, J.S., 2011. Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biology, 11, 5, doi: 10.1186/1471-2229-11-5.
• Sun, G., 2011. MicroRNAs and their diverse functions in plants. Plant Molecular Biology, 18: 17–36.
• Sunkar, R., Kapoor, A., Zhu, J., 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell, 18, 2051–2065.
• Sunkar, R., Chinnusamy, V., Zhu, J., Zhu, J. K. 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Science, 12: 301–309.
• Sunkar, R., Li, Y., Jagadeeswaran, G., 2012. Functions of microRNAs in plant stress Responses. Trends in Plant Science, 17(4): 196-203.
• Tsukagoshi, H., 2016. Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol., 29: 57-63. Tollenaar, M., Lee, E.A. 2002. Yield potential, yield stability and stress tolerance in maize. Field Crops Research, 75: 161–169.
• Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E.F., Hellens, R.P., 2007. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3: 12, doi:10.1186/1746-4811-3-12.
• Wang, W., Xia, M.X., Chen, J., Yuan, R., Deng, F.N., Shen, F.F., 2016. Gene expression characteristics and regulation mechanisms of superoxide dismutase and ıts physiological roles in plants under stress. Biochemistry (Mosc), 81(5): 465-80.
• Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 218: 1–14.
• Zhang, YC, Yu, Y., Wang, C.Y., Li, Z.Y., Liu, Q., Xu, J., Liao, J.Y., Wang, X.J., Qu, L.H., Chen, F., Xin, P., Yan, C., Chu, J., Li, H.Q., Chen, Y.Q., 2013. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol., 31(9): 848-52.
• Jagadeeswaran, G., Saini, A., Sunkar, R., 2009. Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta., 229(4): 1009-14.
• Xie, F.L., Huang, S.Q., Guo, K., Xiang, A.L., Zhu, Y.Y., Nie, L., Yang, Z.M., 2007. Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett., 3;581(7): 1464-1474.
• Hola, D., Kocova, M., Rothova, O., Wilhelmova., N., Benesova, M., 2007. Recovery of maize (Zea mays L.) inbreds and hybrids from chilling stress of various duration: photosynthesis and antioxidant enzymes. J Plant Physiol., 164(7): 868-77.
• Weii L., Zhang, D., Xiang, F., Zhang, Z., 2009. Diferentially expressed miRNAs potentially involved in the regulation of defence mechanism to drought stress in maize seedlings. International Journal of Plant Sciences, 170(8): 979–989.