Horseshoe Adası (Antarktika Yarımadası) ve Türkiye'nin Güney Sahilinden Toplanan Umbilicaria decussata’da MBF-1, PKS ve psbA Genlerinin İfade Varyasyonları

Abstract

Antarktika likenleri, çevresel değişimin göstergesi olarak bilimsel araştırmalara katkıda bulunarak bilim adamlarının iklim değişikliğinin ve insan faaliyetinin etkilerini izlemesine yardımcı olur. Liken türlerinin bu farklı habitatlara ve ekstrem koşullara adaptasyonu, genetik arka planlarındaki genlerin hızlı ekspresyonundan kaynaklanmaktadır. Bu çalışmada Umbilicaria decussata (Vill.) Zahlbr. liken örnekleri Antarktika Yarımadası'nın batısında yer alan Horseshoe Adası'ndan ve Türkiye'nin güney kıyısından olmak üzere iki farklı bölgeden toplandı. Örneklerin nrITS gen bölgeleri incelenmiş ve örneklerin filogenetik pozisyonlarının U. decussata olduğu doğrulanmıştır. DNA barkodlaması sonrasında, multiprotein bağlama faktörü-1 (MBF-1), poliketid sentaz (PKS) ve fotosistem II D1 proteini (psbA) genlerinin sıcaklık değişim stresine bağlı olarak ifadelerindeki meydana gelen değişiklikler qPCR ile karşılaştırmalı olarak tespiti yapılmıştır. Spesifik olarak, Horseshoe Adası'nda olduğu gibi soğuk stresi koşullarında MBF-1 geni yüksek oranda eksprese edilirken, PKS ve psbA gen ekspresyonu seviyeleri Türkiye'nin güney kıyılarına göre daha düşüktü. Farklı coğrafi bölgelerden toplanan örnekler gen ekspresyonu farklılıkları sergilemiştir. Alanında bir ilk olan bu çalışmanın sonuçları, Umbilicaria decussata örneklerinin söz konusu habitatlara ve bölgesel iklime nasıl uyum sağladığının altını çizmektedir.

Keywords

• Antarktika
• İklim değişikliği
• Kutup Biyolojisi
• Gen ekspresyonu
• qRT-PCR

Project Number

121Z771

Expression Variations of MBF-1, PKS and psbA Genes in Umbilicaria decussata Collected from Horseshoe Island (Antarctic Peninsula) and the Southern Coast of Turkiye

Abstract

Antarctic lichens contribute to scientific research as indicators of environmental change, helping scientists monitor the impacts of climate change and human activity. The adaptation of lichen species to these different habitats and extreme conditions is due to rapid in expressions of the genes in their genetic backgrounds. In this study, Umbilicaria decussata (Vill.) Zahlbr. lichen samples were collected with from two different regions: from the Horseshoe Island, located to the west of the Antarctic Peninsula and from the south coast of Turkiye. The nrITS gene regions of the samples were studied and the phylogenetic positions of the samples were confirmed as U. decussata. After DNA barcoding, comparative determinations of the changes in the expressions of the multiprotein binding factor-1 (MBF-1), polyketide synthase (PKS) and photosystem II D1 protein (psbA) genes due to temperature change stress were performed by a qPCR. Specifically, under cold stress conditions such as those found on the Horseshoe Island, the MBF-1 gene was highly expressed, while PKS and psbA gene expression levels were lower compared to the south coast of Turkiye. Specimen collected from different geographical regions exhibited gene expression differences. The results of this study, which is the first in its field, highlight how the adaptation of Umbilicaria decussata samples to those habitats and regional climate.

Keywords

• Antarctica
• Climate change
• Polar biology
• Gene expression
• qRT-PCR

Supporting Institution

This study was conducted under the auspices of the Presidency of the Republic of Turkiye, with support from the Ministry of Industry and Technology. And also, the authors gratefully acknowledge the financial support of this research by Scientific and Technological Research Council of Turkiye (Project No: 121Z771).

Project Number

121Z771

Ethical Statement

There is no need for an ethics committee decision for the studies in the article.

Thanks

The authors thank two anonymous reviewers for their valuable feedback, which helped to improve the manuscript. Additionally, the authors wish to express their gratitude to the Marmara Research Centre (TÜBİTAK-MAM-KARE)-Polar Research Institute and the General Directorate of Meteorology.

References

1. Green, T.A., Schroeter, B., Sancho, L.G. 2007. Plant life in Antarctica. Func. Plant Eco. 1, 389-434. CRC press.
2. Convey, P., Chown, S.L., Clarke, A., Barnes, D.K., Bokhorst, S., Cummings, V., Wall, D.H. 2014. The spatial structure of Antarctic biodiversity. Ecological Monographs 84, 203-244. doi.org/10.1890/12-2216.1
3. Park, C.H., Kim, K.M., Elvebakk, A., Kim, O.S., Jeong, G., Hong, S.G. 2015. Algal and fungal diversity in Antarctic lichens. J. Eukaryot. Microbiol. 62, 196-205. doi.org/10.1111/jeu.12159
4. Halici, M.G., Timdal. E., Möller. E., Bölükbaşı. E., Kahraman-Yiğit, M. 2022a. Rhizocarpon ozsoyae sp. nova (Rhizocarpaceae, lichenized Ascomycetes) from James Ross Island (Antarctic Peninsula). Herzogia 35, 105-114. doi: 10.13158/heia.35.1.2022.105
5. Halici, M.G., Güllü, M., Bölükbaşı, E., Kahraman-Yiğit, M. 2022b. Shackletonia backorii-A new species of lichenised fungus from James Ross Island (Antarctic Peninsula). Turk. J. Bot. 46, 500-506. doi: 10.55730/1300-008X.2725. 10
6. Øvstedal, D.O., Smith, R.I.L. 2001. Lichens of Antarctica and South Georgia: A guide to their identification and ecology. Cambridge University Press. Cambridge.
7. Lamb, I.M. 1948. New rare or interesting lichens from the Southern Hemisphere I. Lilloa, 14, 203-251.
8. Lamb, I.M. 1970. Antarctic terrestrial plants and their ecology. Holdgate, MW Antarctic Ecology.

9. Seppelt, R.D., Nimis, P.L., Castello, M. 1998. The genus Sarcogyne (Acarosporaceae) in Antarctica. The Lichenologist 30, 249-258. doi.org/10.1006/lich.1998.0135
10. Nimis, P.L. 2003. Checklist of the Lichens of Italy 3.0.Trieste: University of Trieste, Department of Biology. http://dbiodbs.univ.trieste.it/, accessed on July 2022.
11. Halici, M.G., Güllü, M., Bölükbaşı, E., Kahraman-Yiğit, M. 2023a. Thamnolecania yunusii (Ramalinaceae)-A new species of lichenised fungus from Horseshoe Island (Antarctic Peninsula). Polar Rec. 59, 1-7. doi:10.1017/S003224742300030X
12. Ying, S.H., Ji, X.P., Wang, X.X., Feng, M.G., Keyhani, N.O. 2014. The transcriptional co-activator multiprotein bridging factor 1 from the fungal insect pathogen, Beauveria bassiana, mediates regulation of hyphal morphogenesis, stress tolerance and virulence. Environ. Microbio. 16, 1879-1897. doi.org/10.1111/1462-2920.12450
13. Qin, D., Wang, F., Geng, X., Zhang, L., Yao, Y., Ni, Z., Sun, Q. 2015. Overexpression of heat stress-responsive TaMBF1c, a wheat (Triticum aestivum L.) Multiprotein Bridging Factor, confers heat tolerance in both yeast and rice. Plant Mol. Bio. 87, 31-45. doi.org/10.1007/s11103-014-0259-9
14. Bölükbaşı, E. 2021. Expression analysis of some stress-related genes induced by cadmium on tomato (S. lycopersicum) plants. Hittite J. Sci. and Engine. 8, 339-345. doi.org/10.17350/HJSE19030000247
15. Zhang, T., Wei, J. 2011. Survival analyses of symbionts isolated from Endocarpon pusillum Hedwig to desiccation and starvation stress. China Life Sci. 54, 480-489. doi.org/10.1007/s11427-011-4164-z
16. Bölükbaşı, E. 2022. Influence of boron treatments on fatty acid desaturase metabolism in different safflower cultivars. Plant, Soil and Environ. 68, 479-486. doi.org/10.17221/228/2022-PSE
17. Zhou, J., Chen, Q., Zhang, Y., Fan, L., Qin, Z., Chen, Q., Zhao, L. 2018. Chitooligosaccharides enhance cold tolerance by repairing photodamaged PS II in rice. J. Agri. Sci. 156, 888-899. doi:10.1017/S0021859618000862
18. Arce, D.P., Godoy, A.V., Tsuda, K., Yamazaki. K., Valle, E.M., Iglesias, M.J., Mauro, M.F.D., Casalongué, C.A. 2010. The analysis of an Arabidopsis triple knock-down mutant reveals functions for MBF1 genes under oxidative stress conditions. J. Plant Physiol. 167, 194-200. doi.org/10.1016/j.jplph.2009.09.003
19. Arce, D.P., Tonón, C., Zanetti, M.E., Godoy, A.V., Hirose, S., Casalongué, C.A. 2006. The potato transcriptional co-activator StMBF1 is up-regulated in response to oxidative stress and interacts with the TATA-box binding protein. J. Biochem. Mol. Biol. 39, 355-360. doi.org/10.5483/BMBRep.2006.39.4.355
20. Wang, Y.Y., Wei, X.L., Huang, J.P., Wei, J.C. 2017a. Modification and functional adaptation of the MBF1 gene family in the lichenized fungus Endocarpon pusillum under environmental stress. Sci. Rep. 7, 16333. doi.org/10.1038/s41598-017-16716-4
21. Gagunashvili, A.N., Davíðsson, S.P., Jónsson, Z.O., Andrésson, Ó.S. 2009. Cloning and heterologous transcription of a polyketide synthase gene from the lichen Solorina crocea. Mycological Res. 113, 354-363. doi.org/10.1016/j.mycres.2008.11.011
22. Timsina, B.A., Hausner, G., Piercey-Normore, M.D. 2014. Evolution of ketosynthase domains of polyketide synthase genes in the Cladonia chlorophaea species complex (Cladoniaceae). Fungal Bio. 118, 896-909. doi.org/10.1016/j.funbio.2014.08.001
23. Wang, Y., Zhou, X., Hur, J.S., Wang, J. 2014. Isolation and charcterizaiton of a polyketide synthase gene cluster from Usnea longissima. Acta Microbiologica Sinica 54, 770-777. PMID: 25252458
24. Abdel-Hameed, M., Bertrand, R.L., Piercey-Normore, M.D., Sorensen, J.L. 2016. Putative identification of the usnic acid biosynthetic gene cluster by de novo whole-genome sequencing of a lichen-forming fungus. Fungal Bio. 120, 306-316. doi.org/10.1016/j.funbio.2015.10.009
25. Klein, R.R., Mullet, J.E. 1987. Control of gene expression during higher plant chloroplast biogenesis protein synthesis and transcript levels of psbA, psaC, psaB and rblc in dark-grown and illuminated Barley seedlings. J. Biol. Chem. 262, 4341-4348. doi.org/10.1016/S0021-9258(18)61353-5
26. Mulo, P., Sicora, C., Aro, E.M. 2009. Cyanobacterial psbA Gene family: Optimization of oxygenic photosynthesis. Cell. Mol. Life. Sci. 66, 3697-3710. doi.org/10.1007/s00018-009-0103-6
27. Kos, P.B., Deak, Z., Cheregi, O., Vass, I. 2008. Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777, 74-83. doi.org/10.1016/j.bbabio.2007.10.015
28. Sander, J., Nowaczyk, M., Kopczak, M., Rögner, M. 2008. Role of the psbA gene family of PSII from the thermophilic cyanobacterium Thermosynechococcus elongatus. In Photosynthesis. Energy from the Sun. 14th International Congress on Photosynthesis 1, 745-748. Springer Netherlands.
29. Qian, H., Li, J., Sun, L., Chen, W., Sheng, G.D., Liu, W., Fu, Z. 2009. Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-relatedgene transcription. Aquat. Toxicol. 94, 56-61. doi.org/10.1016/j.aquatox.2009.05.014 30,31,32
30. Kamitani, M., Nagano, A.J., Honjo, M.N., Kudoh, H., 2016. RNA-Seq reveals virüs-virus and virüs-plant interactions in nature. J. Microbiol. Ecol. 92, 176. doi:10.1093/femsec/fiw176
31. Honjo, M.N., Emura, N., Kawagoe, T., Sugisaka, J., Kamitani, M., Nagano, A.J., 2020. Seasonality of interactions between a plant virus and its host during persistent infection in a natural environment. J. Microbiol. Eco. 14, 506-518. doi:10.1038/ s41396-019-0519-4
32. Hamim, I., Suzuki, J.Y., Borth, W.B., Melzer, M.J., Wall, M.M., Hu, J.S., 2022. Preserving plant samples from remote locations for detection of RNA and DNA viruses. Frontiers in Microbio. 13, 930329. doi:10.3389/fmicb.2022.930329
33. Gardes, M., Bruns, T.D. 1993. ITS primers with enhanced specificity for basidiomycetes14 application to the identification of mycorrhizae and rusts. Mol. Eco. 2, 113-118. doi: 10.1111/j.1365-294x.1993.tb00005.x
34. Seymour, F., Crittenden, P., Wirtz, N., Øvstedal, D., Dyer, P., Lumbsch, H. 2007. Phylogenetic and morphological analysis of Antarctic lichen-forming Usnea species in the group Neuropogon. Antarctic Sci. 19, 71-82. doi: 10.1017/S0954102007000107
35. White, T. J., Bruns, T., Lee, S., Taylor, J. 1990. Amplification and direct sequencing of fungal 7 ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (eds.) PCR protocols: A guide to methods and applications. Academic Press 1, 315-322.
36. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Bio. 215, 403-410. doi.org/10.1016/S0022-2836(05)80360-2
37. Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic acids symposium series 41, 95-98, London Information Retrieval Ltd.
38. Tamura, K., Stecher, G., Kumar, S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Bio. and Evo. 38, 3022-3027. doi.org/10.1093/molbev/msab120
39. Kim, D.G., Lee, C., Park, S.M., Choi, Y.E. 2014. Manipulation of light wavelength at appropriate growth stage to enhance biomass productivity and fatty acid methyl ester yield using Chlorella vulgaris. Bioresource Techno. 159, 240-248. doi.org/10.1016/j.biortech.2014.02.078
40. Sen, G., Eryilmaz, I.E., Ozakca, D. 2014. The effect of aluminium-stress and exogenous spermidine on chlorophyll degradation, glutathione reductase activity and the photosystem II D1 protein gene (psbA) transcript level in lichen Xanthoria parietina. Phytochem. 98, 54-59. doi.org/10.1016/j.phytochem.2013.11.021
41. Livak, J.K., Schmittgen, D.T. 2001. Analysis of relative gene expression data using Real-Time Quantitative PCR and the 2-ΔΔCt method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
42. Kubista, M., Andrade, J.M., Bengtsson, M., Forootan, A., Jonak, J. 2006. The real-time polymerase chain reaction. Mol. Aspects Med. 2, 95-125. doi:10.1016/j.mam.2005.12.007
43. Barták, M., Váczi, P., Hájek, J. 2007. Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans. Polar Bio. 31, 47-51. doi.org/10.1007/s00300-007-0331-x
44. Kyriatzi, A., Tzivras, G., Pirintsos, S., Kotzabasis, K. 2021. Biotechnology under extreme conditions: Lichens after extreme UVB radiation and extreme temperatures produce large amounts of hydrogen. J. Biotech. 342, 128-138. doi.org/10.1016/j.jbiotec.2021.10.011.
45. Da Silva, M.K., Da Silva, A.V., Fernandez, P.M., Montone, R.C., Alves, R.P., De Queiroz, A.C., Duarte, A.W. 2022. Extracellular hydrolytic enzymes produced by yeasts from Antarctic lichens. Anais da Academia Brasileira de Ciências 94. doi 10.1590/0001-3765202220210540
46. Halici, M.G., Kahraman-Yiğit, M., Bölükbaşı, E., Güllü, M. 2023b. New record and new species of lichenized fungal genus Candelariella Müll. Arg. in Antarctica. Polish Polar Res. 44, 1-15. 10.24425/ppr.2023.144537
47. Bölükbaşı, E., Halıcı, M.G. 2024. Molecular signatures of environmental adaptation mechanisms of Rhizocarpon geographicum in Horseshoe Island (west of the Antarctic Peninsula) and Türkiye. Polar Science, 101134.
48. McCarthy, P., Elix, J. 2014. The lichen genus Rhizocarpon in mainland Australia. Telopea 16, 195-211. doi.org/10.7751/telopea20148124
49. Roca-Valiente, B., Hawksworth, D., Pérez-Ortega. S. 2016. Type studies in the Rhizocarpon geographicum group (Rhizocarpaceae, lichenized Ascomycota). The Lichenologist 48(2) 97-110. doi:10.1017/S002428291500050X
50. Wang, Y.Y., Liu, R.D., Wang, W.C., Wei, X., Wei, J. 2017b. Nucleotide differences in the MBF-1 gene of the lichenized fungus Umbilicaria decussata collected in polar and non-polar regions. Adv. Polar Sci. 28, 43-49. doi.org 10.13679/j.advps.2017.1.00043
51. Suzuki, N., Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Mittler, R. 2005. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physio. 139, 1313-1322. doi.org/10.1104/pp.105.070110
52. Ma, Z., Tan, Y., Cui, G., Feng, Y., Cui, Q., Song, X. 2015. Transcriptome and gene expression analysis of DHA producer Aurantiochytrium under low temperature conditions. Sci. Rep. 5, 1-13. doi:10.1038/srep14446
53. Kraft, M., Scheidegger, C., Werth, S. 2022. Stressed out: The effects of heat stress and parasitism on gene expression of the lichen-forming fungus Lobaria pulmonaria. The Lichenologist 54, 71-83. doi:10.1017/S0024282921000463
54. Zhuang, K., Kong, F., Zhang, S., Meng, C., Yang, M., Liu, Z., Wang, Y., Ma, N., Meng, Q. 2019. Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. New Phytol. 221, 1998-2012.
55. Zhuang, K., Wang, J., Jiao, B., Chen, C., Zhang, J., Ma, N., Meng, Q. 2020. SlWHIRLY1 maintains leaf photosynthetic capacity in tomato by regulating the expression of SlRbcS1 under chilling stress. J. Exp. Bot. 71, 3653-3663.
56. Allakhverdiev, S.I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., Murata, N. 2002. Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol. 130, 1443-1453. doi.org/10.1104/pp.011114
57. Rogalski, M., Schottler, M.A., Thiele, W., Schulze, W.X., Bock, R. 2008. Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. The Plant Cell 20, 2221-2237. doi.org/10.1105/tpc.108.060392