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Adaptations in Halophytic Seeds

Year 2023, Volume: 4 Issue: 1, 60 - 78, 15.06.2023

Alper Durmaz Hasan Korkmaz Mehtap Boyraz

https://doi.org/10.53803/turvehab.1215056

Abstract

In order to ensure their continuity in saline habitats, halophyte plants have developed many anatomical, morphological, and physiological adaptations in their seeds, which is one of their basic organs in generative reproduction, as well as the adaptation mechanisms they have developed in other organs. Because none of the adaptive mechanisms they have developed in their vegetative structure can be functional during the germination period of the seed, halophytes have to develop adaptive strategies that will ensure their successful germination, especially in saline habitats. Basically, all adaptive mechanisms for maintaining embryo viability and achieving successful dormancy/germination regulation are due to heterogeneity in seeds. In this way, halophytes have developed adaptive strategies that enable them to survive by successfully germinating despite unpredictable changes in saline habitat conditions. In this review, we tried to explain the anatomical, morphological, physiological, etc. adaptations in the seeds of halophyte species by giving examples from different species.

Keywords

halophyte seed adaptation polymorphism

References

  • Anderson, T.M., Schütz, M. & Risch, A.C. (2012). Seed germination cues and the importance of the soil seed bank across an environmental gradient in the Serengeti. Oikos 121(2): 306312. DOI: https://doi.org/10.1111/j.1600-0706.2011.19803.x.
  • Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., Zohaib, A., Abbas, F., Saleem, M.F., Ali, I. & Wang, L.C. (2017). Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8: 69. DOI: https://doi.org/10.3389/fpls.2017.00069.
  • Apse, M.P. & Blumwald, E. (2007). Na+ transport in plants. FEBS Lett 581(12): 2247–2254. DOI: https://doi.org/10.1016/j.febslet.2007.04.014.
  • Avashthi, H., Pathak, R.K., Pandey, N., Arora, S., Mishra, A.K., Gupta, V. K., Ramteke, P.W. & Kumar, A. (2018). Transcriptome-wide identification of genes involved in Ascorbate–Glutathione cycle (Halliwell–Asada pathway) and related pathway for elucidating its role in antioxidative potential in finger millet (Eleusine coracana (L.). 3 Biotech 8(12): 118. DOI: https://doi.org/10.1007/s13205-018-1511-9.
  • Baskin, C.C. & Baskin, J.M. (2014). Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. 2nd Edn. Elsevier, San Diego.
  • Beisson, F., Li, Y., Bonaventure, G., Pollard, M. & Ohlrogge, J.B. (2007). The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19(1): 351368. DOI: https://doi.org/10.1105/tpc.106.048033.
  • Bewley, J.D., Bradford, K.J., Hilhorst, H.W. & Nonogaki, H. (2013). Environmental Regulation of Dormancy and Germination. Springer, New York, pp. 299–339.
  • Boyraz, M., Korkmaz, H. & Durmaz, A. (2019). Tohumda dormansi ve çimlenme. Black Sea Journal of Engineering and Science 2(3): 92105. DOI: https://doi.org/10.34248/bsengineering. 527684.
  • Cao, D., Baskin, C.C., Baskin, J.M., Yang, F. & Huang, Z. (2012). Comparison of germination and seed bank dynamics of dimorphic seeds of the cold desert halophyte Suaeda corniculata subsp. mongolica. Ann Bot 110(8): 15451558. DOI: https://doi.org/10.1093/aob/mcs205.
  • Cao, D., Baskin, C.C., Baskin, J.M., Yang, F. & Huang, Z. (2014). Dormancy cycling and persistence of seeds in soil of a cold desert halophyte shrub. Ann Bot 113(1): 171–179. DOI: https://doi.org/10.1093/aob/mct256.
  • Cao, J., Lv, X.Y., Chen, L., Xing, J.J. & Lan, H.Y. (2015). Effects of salinity on the growth, physiology and relevant gene expression of an annual halophyte grown from heteromorphic seeds. AoB Plants 7: 112. DOI: https://doi.org/10.1093/aobpla/plv112.
  • Cao, J., Wang, L. & Lan, H. (2016). Validation of reference genes for quantitative RT-PCR normalization in Suaeda aralocaspica, an annual halophyte with heteromorphism and C4 pathway without Kranz anatomy. PeerJ 4: e1697. DOI: https://doi.org/10.7717/peerj.1697.
  • Caparrós, P.G., Öztürk, M., Gul, A., Batool, T.S., Pirasteh-Anosheh, H., Ünal, B.T., Altay, V. & Toderich, K.N. (2022). Halophytes have potential as heavy metal phytoremediators: A comprehensive review. Environ Exp Bot 193: 104666. DOI: https://doi.org/10.1016/ j.envexpbot.2021.104666.
  • Debez, A., Belghith, I., Pich, A., Taamalli, W., Abdelly, C. & Braun, H.P. (2018). High salinity impacts germination of the halophyte Cakile maritima but primes seeds for rapid germination upon stress release. Physiol Plant 164(2): 134144. DOI: https://doi.org/ 10.1111/ppl.12679.
  • El-Keblawy, A., Gairola, S. & Bhatt, A. (2016). Maternal habitat affects germination requirements of Anabasis setifera, a succulent shrub of the Arabian deserts. Acta Botanica Brasilica 30(1): 3540. DOI: https://doi.org/10.1590/0102-33062015abb0212.
  • Fukuhara, T., Kirch, H.H. & Bohnert, H.J. (1999). Expression of Vp1 and water channel proteins during seed germination. Plant Cell Environ 22(4): 417424. DOI: https://doi.org/10.1046/ j.1365-3040.1999.00427.x.
  • Gao, H.J., Lü, X.P., Zhang, L., Qiao, Y., Zhao, Q., Wang, Y.P., Li, M.F. & Zhang, J.L. (2018). Transcriptomic profiling and physiological analysis of haloxylon ammodendron in response to osmotic stress. Int J Mol Sci 19(1): 84. DOI: https://doi.org/10.3390/ijms19010084.
  • González, M.B. (2019). [Adaptation of halophytes to different habitats]. In: Jimenez-Lopez, J.C. (Ed.). Seed Dormancy and Germination. IntechOpen. DOI: 10.5772/intechopen.87056.
  • Grigore M.N. (2012). Romanian salt tolerant plants. Taxonomy and ecology. Iaşi, Edit. Tehnopress.
  • Guja, L., Wuhrer, R., Moran, K., Dixon, K.W., Wardell-Johnson, G. & Merritt, D.J. (2013). Full spectrum X-ray mapping reveals differential localization of salt in germinating seeds of differing salt tolerance. Bot J Linn Soc 173(1): 129142. DOI: https://doi.org/ 10.1111/boj.12072.
  • Gul, B., Ansari, R., Flowers, T.J. & Khan, M.A. (2013). Germination strategies of halophyte seeds under salinity. Environ Exp Bot 92(1): 418. DOI: https://doi.org/10.1016/ j.envexpbot.2012.11.006.
  • Guo, J., Suo, S. & Wang, B.S. (2015). Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Sci Res 25(3): 335344. DOI: https://doi.org/10.1017/ S0960258515000239.
  • Hasanuzzaman, M., Nahar, K. & Öztürk, M. (2019). Ecophysiology, Abiotic Stress Responses and Utilization of Halophytes. Springer, New York.
  • Imbert, E. (2002). Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 5(1): 1336. DOI: https://doi.org/10.1078/1433-8319-00021.
  • İç, S. (2015). Çarşamba Ovası Sol Sahil Topraklarında Yorgunluk Parametrelerinin Belirlenmesi (Doktora Tezi). Ondokuz Mayıs Üniversitesi, Fen Bilimleri Enstitüsü, Samsun.
  • Jaimand, K. & Rezaee, M.B. (1996). Variability in seed composition due to plant population and capitula zones of sunflower. Agrochimica 40: 48–54.
  • Kazachkova, Y., Khan, A., Acuña, T., López-Díaz, I., Carrera, E., Khozin-Goldberg, I., Fait, A. & Barak, S. (2016). Salt induces features of a dormancy-like state in seeds of Eutrema (Thellungiella) salsugineum, a halophytic relative of Arabidopsis. Front Plant Sci 7: 1071. DOI: https://doi.org/10.3389/fpls.2016.01071.
  • Khan, M.A. & Gul, B. (1998). High salt tolerance in germinating dimorphic seeds of Arthrocnemum indicum. Int J Plant Sci 159(5): 826832. DOI: https://doi.org/10.1086/297603.
  • Khan, M.A., Ansari, R., Gul, B. & Li, W. (2009). Dormancy and germination responses of halophyte seeds to the application of ethylene. C R Biol 332(9): 806815. DOI: https://doi.org/10.1016/ j.crvi.2009.05.002.
  • Kochánková, J. & Mandák, B. (2009). How do population genetic parameters affect germination of the heterocarpic species Atriplex tatarica (Amaranthaceae)? Ann Bot 103(8): 13031313. DOI: https://doi.org/10.1093/aob/mcp073.
  • Kucera, B., Cohn, M.A. & Leubner-Metzger, G. (2005). Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15(4): 281307. DOI: https://doi.org/ 10.1079/SSR2005218.
  • Kumari, A., Das, P., Parida, A.K. & Agarwal, P.K. (2015). Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6: 537. DOI: https://doi.org/10.3389/fpls.2015.00537.
  • Lee, Y.P., Funk, C., Erban, A., Kopka, J., Köhl, K.I., Zuther, E. & Hincha, D.K. (2016). Salt stress responses in a geographically diverse collection of Eutrema/Thellungiella spp. accessions. Funct Plant Biol 43(7): 590606. DOI: https://doi.org/10.1071/FP15285.
  • Lenser, T., Graeber, K., Çevik, Ö.S., Adıgüzel, N., Dönmez, A.A., Grosche, C., Kettermann, M., Mayland-Quellhorst, S., Mérai, Z., Mohammadin, S., Nguyen, T.P., Rümpler, F., Schulze, C., Sperber, K., Steinbrecher, T., Wiegand, N., Strnad, M., Scheid, O.M., Rensing, S.A., Schranz, M.E., Theißen, G., Mummenhoff, K. & Leubner-Metzger, G. (2016). Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum. Plant Physiol 172(3): 1691–1707. DOI: https://doi.org/10.1104/pp. 16.00838.
  • Li, W., Liu, X., Khan, M.A. & Yamaguchi, S. (2005). The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J Plant Res 118(3): 207214. DOI: https://doi.org/10.1007/s10265-005-0212-8.
  • Li, W., An, P., Liu, X., Khan, M.A., Tsuji, W. & Tanaka, K. (2008). The effect of light, temperature and bracteoles on germination of polymorphic seeds of Atriplex centralasiatica Iljin under saline conditions. Seed Science and Technology 36(2): 325.
  • Li, X., Zhang, X., Song, J., Fan, H., Feng, G. & Wang, B. (2011). Accumulation of ions during seed development under controlled saline conditions of two Suaeda salsa populations is related to their adaptation to saline environments. Plant Soil 341(1): 99107. DOI: https://doi.org/ 10.1007/s11104-010-0625-6.
  • Li, W., Yamaguchi, S., Khan, M.A., An, P., Liu, X., & Tran, L.S.P. (2016a). Roles of gibberellins and abscisic acid in regulating germination of Suaeda salsa dimorphic seeds under salt stress. Front Plant Sci 6: 1235. DOI: https://doi.org/10.3389/fpls.2015.01235.
  • Li, Z., Zhang, J., Li, J., Li, H. & Zhang, G. (2016b). The functional and regulatory mechanisms of the Thellungiella salsuginea ascorbate peroxidase 6 (TsAPX6) in response to salinity and water deficit stresses. PLoS One 11(4): e0154042. DOI: https://doi.org/10.1371/ journal.pone.0154042
  • Linkies, A., Graeber, K., Knight, C. & Leubner‐Metzger, G. (2010). The evolution of seeds. New Phytol 186(4): 817831. DOI: 10.1111/j.1469-8137.2010.03249.x.
  • Liu, R., Wang, L., Tanveer, M. & Song, J. (2018). Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity. Front Plant Sci 9: 1515. DOI: https://doi.org/10.3389/ fpls.2018.01515.
  • Lloyd, D.G. (1984). Variation strategies of plants in heterogeneous environments. Biol J Linn Soc 21(4): 357–385. DOI: https://doi.org/10.1111/j.1095-8312.1984.tb01600.x.
  • Ludewig, K., Zelle, B., Eckstein, R.L., Mosner, E., Otte, A. & Donath, T.W. (2014). Differential effects of reduced water potential on the germination of floodplain grassland species indicative of wet and dry habitats. Seed Sci Res 24(1): 4961. DOI: https://doi.org/ 10.1017/S096025851300038X.
  • Ma, Y., Wang, J., Zhang, J., Zhang, S., Liu, Y. & Lan, H. (2018). Seed heteromorphism and effects of light and abiotic stress on germination of a typical annual halophyte Salsola ferganica in cold desert. Front Plant Sci 8: 2257. DOI: https://doi.org/10.3389/fpls.2017.02257.
  • Maxwell, C.D, Zobel, A. & Woodfine, D. (1994). Somatic polymorphism in the achenes of Tragopogon dubius. Can J Bot 72(9): 1282–1288. DOI: https://doi.org/10.1139/b94-156.
  • Mohamed, E., Kasem, A.M. & Farghali, K.A. (2018). Seed germination of Egyptian Pancratium maritimum under salinity with regard to cytology, antioxidant and reserve mobilization enzymes, and seed anatomy. Flora 242: 120127. DOI: https://doi.org/10.1016/ j.flora.2018.03.011.
  • Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytol 167(3): 645663.
  • Noctor, G., Mhamdi, A., Chaouch, S., Han, Y.I., Neukermans, J., Marquez‐Garcia, B., Queval, G. & Foyer, C.H. (2012). Glutathione in plants: an integrated overview. Plant Cell Environ 35(2): 454484. DOI: 10.1111/j.1365-3040.2011.02400.x.
  • Orlovsky, N., Japakova, U., Zhang, H. & Volis, S. (2016). Effect of salinity on seed germination, growth and ion content in dimorphic seeds of Salicornia europaea L. (Chenopodiaceae). Plant Divers 38(4): 183189. DOI: https://doi.org/10.1016/j.pld.2016.06.005.
  • Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y. & Lopez-Molina, L. (2008). The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20(10): 27292745. DOI: https://doi.org/10.1105/tpc.108.061515.
  • Pujol, J.A., Calvo, J.F. & Ramirez-Diaz, L. (2000). Recovery of germination from different osmotic conditions by four halophytes from southeastern Spain. Ann Bot 85(2): 279286. DOI: https://doi.org/10.1006/anbo.1999.1028.
  • Shabala, S., Cuin, T.A. & Pottosin, I. (2007). Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581(10): 19931999. DOI: https://doi.org/10.1016/j.febslet.2007.04.032.
  • Sharma, A., Devi, A., Garg, C., Kumari, A., Mann, A. & Kumar, A. (2019). Behavior of Halophytes and Their Tolerance Mechanism Under Different Abiotic Stresses. In Ecophysiology, Abiotic Stress Responses and Utilization of Halophytes. Springer, Singapore, pp. 2538.
  • Shen, Y.Y., Li, Y. & Yan, S.G. (2003). Effects of salinity on germination of six salt‐tolerant forage species and their recovery from saline conditions. N Z J Agric Res 46(3): 263269. DOI: https://doi.org/10.1080/00288233.2003.9513552.
  • Song, J. & Wang, B. (2015). Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115(3): 541553. DOI: https://doi.org/10.1093/aob/mcu194.
  • Song, J., Feng, G.U., Tian, C. & Zhang, F. (2005). Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Ann Bot 96(3): 399405. DOI: https://doi.org/10.1093/aob/mci196.
  • Song, J., Feng, G., Li, Z.K., Chen, A.D., Chen, X.M. & Zhang, F.S. (2007). Effects of salinity and scarifying seed coat on ion content of embryos and seed germination for Suaeda physophora and Haloxylon ammodendron. Seed Science and Technology 35(3): 615623. DOI: https://doi.org/10.15258/sst.2007.35.3.09.
  • Song, J., Fan, H., Zhao, Y., Jia, Y., Du, X. & Wang, B. (2008). Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquat Bot 88(4): 331337. DOI: https://doi.org/10.1016/j.aquabot.2007.11.004.
  • Song, J., Zhou, J., Zhao, W., Xu, H., Wang, F., Xu, Y., Wang, L. & Tian, C. (2016). Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biol 31(1): 1928. DOI: https://doi.org/10.1111/1442-1984.12071.
  • Song, J., Shi, W., Liu, R., Xu, Y., Sui, N., Zhou, J. & Feng, G. (2017). The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol 32(2): 107114. DOI: https://doi.org/10.1111/1442-1984.12132.
  • Sui, N., Li, M., Li, K., Song, J. & Wang, B.S. (2010). Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48(4): 623629. DOI: https://doi.org/10.1007/s11099-010-0080-x.
  • Sui, N. & Han, G. (2014). Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiol Plant 36(4): 983992. DOI: https://doi.org/10.1007/s11738-013-1477-5.
  • Sui, N., Tian, S., Wang, W., Wang, M. & Fan, H. (2017). Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Front Plant Sci 8: 1337. DOI: https://doi.org/10.3389/fpls.2017.01337.
  • Tada, Y., Kawano, R., Komatsubara, S., Nishimura, H., Katsuhara, M., Ozaki, S., Terashima, S., Yano, K., Endo, C., Sato, M., Okamoto, M., Sawada, Y., Hirai, M.Y. & Kurusu, T. (2019). Functional screening of salt tolerance genes from a halophyte Sporobolus virginicus and transcriptomic and metabolomic analysis of salt tolerant plants expressing glycine-rich RNA-binding protein. Plant Sci 278: 5463. DOI: https://doi.org/0.1016/ j.plantsci.2018.10.019.
  • Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K., Narusaka, Y., Narusaka, M., Zhu, J.K. & Shinozaki, K. (2004). Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135(^):1697–1709. DOI: https://doi.org/10.1104/pp.104.039909.
  • Tanveer, M. & Shah, A.N. (2017). An insight into salt stress tolerance mechanisms of Chenopodium album. Environ Sci Pollut Res 24: 16531–16535. DOI: 10.1007/s11356-017-9337-2.
  • Tuteja, N. (2007). Mechanisms of high salinity tolerance in plants. Methods Enzymol 428: 419438.
  • Wang, H.L., Wang, L., Tian, C.Y. & Huang, Z.Y. (2012). Germination dimorphism in Suaeda acuminata: a new combination of dormancy types for heteromorphic seeds. S Afr J Bot 78: 270275. DOI: https://doi.org/10.1016/j.sajb.2011.05.012.
  • Wang, F., Xu, Y.G., Wang, S., Shi, W., Liu, R., Feng, G. & Song, J. (2015). Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol Biochem 95: 4148. DOI: https://doi.org/10.1016/j.plaphy.2015.07.005.
  • Wang, F.X., Yin, C.H., Song, Y.P., Li, Q., Tian, C.Y. & Song, J. (2018). Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions. Plant Biosyst - Int J Dealing Aspects Plant Biosyst 152(4): 749758. DOI: https://doi.org/10.1080/ 11263504.2017.1330776.
  • Xu, Y., Zhao, Y., Duan, H., Sui, N., Yuan, F. & Song, J. (2017). Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa. BMC Genomics 18(1), 114. DOI: https://doi.org/10.1186/s12864-017-4104-9.
  • Yan, C., Wei, Y. & Yang, M. (2011). Comparative germination of Tamarix ramosissima spring and summer seeds. EXCLI journal 10: 198.
  • Yuan, K., Rashotte, A.M., & Wysocka-Diller, J.W. (2011). ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiol Plant 33(2): 261271. DOI: https://doi.org/10.1007/s11738-010-0542-6.
  • Yuan, F., Guo, J., Shabala, S. & Wang, B. (2019). Reproductive physiology of halophytes: current standing. Front Plant Sci 9: 1954. DOI: https://doi.org/10.3389/fpls.2018.01954.
  • Zhang, H., Zhang, G., Lü, X., Zhou, D. & Han, X. (2015). Salt tolerance during seed germination and early seedling stages of 12 halophytes. Plant Soil 388(1): 229241. DOI: https://doi.org/10.1007/s11104-014-2322-3.
  • Zhang, H., Zhu, J., Gong, Z. & Zhu, J. K. (2022). Abiotic stress responses in plants. Nat Rev Genet 23(2): 104119. DOI: https://doi.org/10.1038/s41576-021-00413-0.
  • Zhang, S., Song, J., Wang, H. & Feng, G. (2010). Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia. J Plant Ecol 3(4): 259267. DOI: https://doi.org/10.1093/jpe/rtq005.
  • Zhang, X., Liao, M., Chang, D. & Zhang, F. (2014). Comparative transcriptome analysis of the Asteraceae halophyte Karelinia caspica under salt stress. BMC Res Notes 7(1): 927. DOI: https://doi.org/10.1186/1756-0500-7-927.
  • Zhao, Y., Yang, Y., Song, Y., Li, Q. & Song, J. (2018). Analysis of storage compounds and inorganic ions in dimorphic seeds of euhalophyte Suaeda salsa. Plant Physiol Biochem 130: 511516. DOI: https://doi.org/10.1016/j.plaphy.2018.08.003.
  • Zhou, C., Sun, Y., Ma, Z. & Wang, J. (2015). Heterologous expression of EsSPDS1 in tobacco plants improves drought tolerance with efficient reactive oxygen species scavenging systems. S Afr J Bot 96: 1928. DOI: https://doi.org/10.1016/j.sajb.2014.10.008.
  • Zhou, J.C., Fu, T.T., Sui, N., Guo, J.R., Feng, G., Fan, J.L. & Song, J. (2016). The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst - Int J Dealing Aspects Plant Biosyst 150(1): 8390. DOI: https://doi.org/10.1080/11263504.2014.976294.

Halofitik Tohumlarda Adaptasyonlar

Year 2023, Volume: 4 Issue: 1, 60 - 78, 15.06.2023

Alper Durmaz Hasan Korkmaz Mehtap Boyraz

https://doi.org/10.53803/turvehab.1215056

Abstract

Halofit bitkiler tuzlu habitatlarda devamlılıklarını sağlamak için, diğer organlarında geliştirdikleri adaptasyon mekanizmalarının yanında, generatif çoğalmadaki temel organlarından tohumlarında da birçok anatomik, morfolojik, fizyolojik vs. nitelikte mekanizmalar geliştirmişlerdir. Çünkü vejetatif yapılarında geliştirdikleri adaptif mekanizmaların hiçbiri, tohumun çimlenme döneminde fonksiyonel olamayacağı için halofitler, özellikle tuzlu habitatlarda başarılı çimlenmelerini sağlayacak, adaptif stratejiler geliştirmek zorundadırlar. Temel olarak, embriyonun canlılığının korunması ve başarılı bir dormansi/çimlenme düzenlemesinin sağlanmasına yönelik tüm adaptif mekanizmalar, tohumlardaki heterojeniteden kaynaklanmaktadır. Halofitler bu sayede, tuzlu habitat şartlarındaki öngörülemeyen değişikliklere rağmen başarılı çimlenmelerini gerçekleştirerek, hayatta kalmalarını sağlayan adaptif stratejiler geliştirmişlerdir. Biz bu derlemede halofit türlerin tohumlarında oluşan anatomik, morfolojik, fizyolojik vs. nitelikteki adaptasyonları, farklı türlerden örnekler vererek açıklamaya çalıştık.

Keywords

halofit tohum adaptasyon polimorfizm

References

  • Anderson, T.M., Schütz, M. & Risch, A.C. (2012). Seed germination cues and the importance of the soil seed bank across an environmental gradient in the Serengeti. Oikos 121(2): 306312. DOI: https://doi.org/10.1111/j.1600-0706.2011.19803.x.
  • Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., Zohaib, A., Abbas, F., Saleem, M.F., Ali, I. & Wang, L.C. (2017). Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8: 69. DOI: https://doi.org/10.3389/fpls.2017.00069.
  • Apse, M.P. & Blumwald, E. (2007). Na+ transport in plants. FEBS Lett 581(12): 2247–2254. DOI: https://doi.org/10.1016/j.febslet.2007.04.014.
  • Avashthi, H., Pathak, R.K., Pandey, N., Arora, S., Mishra, A.K., Gupta, V. K., Ramteke, P.W. & Kumar, A. (2018). Transcriptome-wide identification of genes involved in Ascorbate–Glutathione cycle (Halliwell–Asada pathway) and related pathway for elucidating its role in antioxidative potential in finger millet (Eleusine coracana (L.). 3 Biotech 8(12): 118. DOI: https://doi.org/10.1007/s13205-018-1511-9.
  • Baskin, C.C. & Baskin, J.M. (2014). Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. 2nd Edn. Elsevier, San Diego.
  • Beisson, F., Li, Y., Bonaventure, G., Pollard, M. & Ohlrogge, J.B. (2007). The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19(1): 351368. DOI: https://doi.org/10.1105/tpc.106.048033.
  • Bewley, J.D., Bradford, K.J., Hilhorst, H.W. & Nonogaki, H. (2013). Environmental Regulation of Dormancy and Germination. Springer, New York, pp. 299–339.
  • Boyraz, M., Korkmaz, H. & Durmaz, A. (2019). Tohumda dormansi ve çimlenme. Black Sea Journal of Engineering and Science 2(3): 92105. DOI: https://doi.org/10.34248/bsengineering. 527684.
  • Cao, D., Baskin, C.C., Baskin, J.M., Yang, F. & Huang, Z. (2012). Comparison of germination and seed bank dynamics of dimorphic seeds of the cold desert halophyte Suaeda corniculata subsp. mongolica. Ann Bot 110(8): 15451558. DOI: https://doi.org/10.1093/aob/mcs205.
  • Cao, D., Baskin, C.C., Baskin, J.M., Yang, F. & Huang, Z. (2014). Dormancy cycling and persistence of seeds in soil of a cold desert halophyte shrub. Ann Bot 113(1): 171–179. DOI: https://doi.org/10.1093/aob/mct256.
  • Cao, J., Lv, X.Y., Chen, L., Xing, J.J. & Lan, H.Y. (2015). Effects of salinity on the growth, physiology and relevant gene expression of an annual halophyte grown from heteromorphic seeds. AoB Plants 7: 112. DOI: https://doi.org/10.1093/aobpla/plv112.
  • Cao, J., Wang, L. & Lan, H. (2016). Validation of reference genes for quantitative RT-PCR normalization in Suaeda aralocaspica, an annual halophyte with heteromorphism and C4 pathway without Kranz anatomy. PeerJ 4: e1697. DOI: https://doi.org/10.7717/peerj.1697.
  • Caparrós, P.G., Öztürk, M., Gul, A., Batool, T.S., Pirasteh-Anosheh, H., Ünal, B.T., Altay, V. & Toderich, K.N. (2022). Halophytes have potential as heavy metal phytoremediators: A comprehensive review. Environ Exp Bot 193: 104666. DOI: https://doi.org/10.1016/ j.envexpbot.2021.104666.
  • Debez, A., Belghith, I., Pich, A., Taamalli, W., Abdelly, C. & Braun, H.P. (2018). High salinity impacts germination of the halophyte Cakile maritima but primes seeds for rapid germination upon stress release. Physiol Plant 164(2): 134144. DOI: https://doi.org/ 10.1111/ppl.12679.
  • El-Keblawy, A., Gairola, S. & Bhatt, A. (2016). Maternal habitat affects germination requirements of Anabasis setifera, a succulent shrub of the Arabian deserts. Acta Botanica Brasilica 30(1): 3540. DOI: https://doi.org/10.1590/0102-33062015abb0212.
  • Fukuhara, T., Kirch, H.H. & Bohnert, H.J. (1999). Expression of Vp1 and water channel proteins during seed germination. Plant Cell Environ 22(4): 417424. DOI: https://doi.org/10.1046/ j.1365-3040.1999.00427.x.
  • Gao, H.J., Lü, X.P., Zhang, L., Qiao, Y., Zhao, Q., Wang, Y.P., Li, M.F. & Zhang, J.L. (2018). Transcriptomic profiling and physiological analysis of haloxylon ammodendron in response to osmotic stress. Int J Mol Sci 19(1): 84. DOI: https://doi.org/10.3390/ijms19010084.
  • González, M.B. (2019). [Adaptation of halophytes to different habitats]. In: Jimenez-Lopez, J.C. (Ed.). Seed Dormancy and Germination. IntechOpen. DOI: 10.5772/intechopen.87056.
  • Grigore M.N. (2012). Romanian salt tolerant plants. Taxonomy and ecology. Iaşi, Edit. Tehnopress.
  • Guja, L., Wuhrer, R., Moran, K., Dixon, K.W., Wardell-Johnson, G. & Merritt, D.J. (2013). Full spectrum X-ray mapping reveals differential localization of salt in germinating seeds of differing salt tolerance. Bot J Linn Soc 173(1): 129142. DOI: https://doi.org/ 10.1111/boj.12072.
  • Gul, B., Ansari, R., Flowers, T.J. & Khan, M.A. (2013). Germination strategies of halophyte seeds under salinity. Environ Exp Bot 92(1): 418. DOI: https://doi.org/10.1016/ j.envexpbot.2012.11.006.
  • Guo, J., Suo, S. & Wang, B.S. (2015). Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Sci Res 25(3): 335344. DOI: https://doi.org/10.1017/ S0960258515000239.
  • Hasanuzzaman, M., Nahar, K. & Öztürk, M. (2019). Ecophysiology, Abiotic Stress Responses and Utilization of Halophytes. Springer, New York.
  • Imbert, E. (2002). Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 5(1): 1336. DOI: https://doi.org/10.1078/1433-8319-00021.
  • İç, S. (2015). Çarşamba Ovası Sol Sahil Topraklarında Yorgunluk Parametrelerinin Belirlenmesi (Doktora Tezi). Ondokuz Mayıs Üniversitesi, Fen Bilimleri Enstitüsü, Samsun.
  • Jaimand, K. & Rezaee, M.B. (1996). Variability in seed composition due to plant population and capitula zones of sunflower. Agrochimica 40: 48–54.
  • Kazachkova, Y., Khan, A., Acuña, T., López-Díaz, I., Carrera, E., Khozin-Goldberg, I., Fait, A. & Barak, S. (2016). Salt induces features of a dormancy-like state in seeds of Eutrema (Thellungiella) salsugineum, a halophytic relative of Arabidopsis. Front Plant Sci 7: 1071. DOI: https://doi.org/10.3389/fpls.2016.01071.
  • Khan, M.A. & Gul, B. (1998). High salt tolerance in germinating dimorphic seeds of Arthrocnemum indicum. Int J Plant Sci 159(5): 826832. DOI: https://doi.org/10.1086/297603.
  • Khan, M.A., Ansari, R., Gul, B. & Li, W. (2009). Dormancy and germination responses of halophyte seeds to the application of ethylene. C R Biol 332(9): 806815. DOI: https://doi.org/10.1016/ j.crvi.2009.05.002.
  • Kochánková, J. & Mandák, B. (2009). How do population genetic parameters affect germination of the heterocarpic species Atriplex tatarica (Amaranthaceae)? Ann Bot 103(8): 13031313. DOI: https://doi.org/10.1093/aob/mcp073.
  • Kucera, B., Cohn, M.A. & Leubner-Metzger, G. (2005). Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15(4): 281307. DOI: https://doi.org/ 10.1079/SSR2005218.
  • Kumari, A., Das, P., Parida, A.K. & Agarwal, P.K. (2015). Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6: 537. DOI: https://doi.org/10.3389/fpls.2015.00537.
  • Lee, Y.P., Funk, C., Erban, A., Kopka, J., Köhl, K.I., Zuther, E. & Hincha, D.K. (2016). Salt stress responses in a geographically diverse collection of Eutrema/Thellungiella spp. accessions. Funct Plant Biol 43(7): 590606. DOI: https://doi.org/10.1071/FP15285.
  • Lenser, T., Graeber, K., Çevik, Ö.S., Adıgüzel, N., Dönmez, A.A., Grosche, C., Kettermann, M., Mayland-Quellhorst, S., Mérai, Z., Mohammadin, S., Nguyen, T.P., Rümpler, F., Schulze, C., Sperber, K., Steinbrecher, T., Wiegand, N., Strnad, M., Scheid, O.M., Rensing, S.A., Schranz, M.E., Theißen, G., Mummenhoff, K. & Leubner-Metzger, G. (2016). Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum. Plant Physiol 172(3): 1691–1707. DOI: https://doi.org/10.1104/pp. 16.00838.
  • Li, W., Liu, X., Khan, M.A. & Yamaguchi, S. (2005). The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J Plant Res 118(3): 207214. DOI: https://doi.org/10.1007/s10265-005-0212-8.
  • Li, W., An, P., Liu, X., Khan, M.A., Tsuji, W. & Tanaka, K. (2008). The effect of light, temperature and bracteoles on germination of polymorphic seeds of Atriplex centralasiatica Iljin under saline conditions. Seed Science and Technology 36(2): 325.
  • Li, X., Zhang, X., Song, J., Fan, H., Feng, G. & Wang, B. (2011). Accumulation of ions during seed development under controlled saline conditions of two Suaeda salsa populations is related to their adaptation to saline environments. Plant Soil 341(1): 99107. DOI: https://doi.org/ 10.1007/s11104-010-0625-6.
  • Li, W., Yamaguchi, S., Khan, M.A., An, P., Liu, X., & Tran, L.S.P. (2016a). Roles of gibberellins and abscisic acid in regulating germination of Suaeda salsa dimorphic seeds under salt stress. Front Plant Sci 6: 1235. DOI: https://doi.org/10.3389/fpls.2015.01235.
  • Li, Z., Zhang, J., Li, J., Li, H. & Zhang, G. (2016b). The functional and regulatory mechanisms of the Thellungiella salsuginea ascorbate peroxidase 6 (TsAPX6) in response to salinity and water deficit stresses. PLoS One 11(4): e0154042. DOI: https://doi.org/10.1371/ journal.pone.0154042
  • Linkies, A., Graeber, K., Knight, C. & Leubner‐Metzger, G. (2010). The evolution of seeds. New Phytol 186(4): 817831. DOI: 10.1111/j.1469-8137.2010.03249.x.
  • Liu, R., Wang, L., Tanveer, M. & Song, J. (2018). Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity. Front Plant Sci 9: 1515. DOI: https://doi.org/10.3389/ fpls.2018.01515.
  • Lloyd, D.G. (1984). Variation strategies of plants in heterogeneous environments. Biol J Linn Soc 21(4): 357–385. DOI: https://doi.org/10.1111/j.1095-8312.1984.tb01600.x.
  • Ludewig, K., Zelle, B., Eckstein, R.L., Mosner, E., Otte, A. & Donath, T.W. (2014). Differential effects of reduced water potential on the germination of floodplain grassland species indicative of wet and dry habitats. Seed Sci Res 24(1): 4961. DOI: https://doi.org/ 10.1017/S096025851300038X.
  • Ma, Y., Wang, J., Zhang, J., Zhang, S., Liu, Y. & Lan, H. (2018). Seed heteromorphism and effects of light and abiotic stress on germination of a typical annual halophyte Salsola ferganica in cold desert. Front Plant Sci 8: 2257. DOI: https://doi.org/10.3389/fpls.2017.02257.
  • Maxwell, C.D, Zobel, A. & Woodfine, D. (1994). Somatic polymorphism in the achenes of Tragopogon dubius. Can J Bot 72(9): 1282–1288. DOI: https://doi.org/10.1139/b94-156.
  • Mohamed, E., Kasem, A.M. & Farghali, K.A. (2018). Seed germination of Egyptian Pancratium maritimum under salinity with regard to cytology, antioxidant and reserve mobilization enzymes, and seed anatomy. Flora 242: 120127. DOI: https://doi.org/10.1016/ j.flora.2018.03.011.
  • Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytol 167(3): 645663.
  • Noctor, G., Mhamdi, A., Chaouch, S., Han, Y.I., Neukermans, J., Marquez‐Garcia, B., Queval, G. & Foyer, C.H. (2012). Glutathione in plants: an integrated overview. Plant Cell Environ 35(2): 454484. DOI: 10.1111/j.1365-3040.2011.02400.x.
  • Orlovsky, N., Japakova, U., Zhang, H. & Volis, S. (2016). Effect of salinity on seed germination, growth and ion content in dimorphic seeds of Salicornia europaea L. (Chenopodiaceae). Plant Divers 38(4): 183189. DOI: https://doi.org/10.1016/j.pld.2016.06.005.
  • Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y. & Lopez-Molina, L. (2008). The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20(10): 27292745. DOI: https://doi.org/10.1105/tpc.108.061515.
  • Pujol, J.A., Calvo, J.F. & Ramirez-Diaz, L. (2000). Recovery of germination from different osmotic conditions by four halophytes from southeastern Spain. Ann Bot 85(2): 279286. DOI: https://doi.org/10.1006/anbo.1999.1028.
  • Shabala, S., Cuin, T.A. & Pottosin, I. (2007). Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581(10): 19931999. DOI: https://doi.org/10.1016/j.febslet.2007.04.032.
  • Sharma, A., Devi, A., Garg, C., Kumari, A., Mann, A. & Kumar, A. (2019). Behavior of Halophytes and Their Tolerance Mechanism Under Different Abiotic Stresses. In Ecophysiology, Abiotic Stress Responses and Utilization of Halophytes. Springer, Singapore, pp. 2538.
  • Shen, Y.Y., Li, Y. & Yan, S.G. (2003). Effects of salinity on germination of six salt‐tolerant forage species and their recovery from saline conditions. N Z J Agric Res 46(3): 263269. DOI: https://doi.org/10.1080/00288233.2003.9513552.
  • Song, J. & Wang, B. (2015). Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115(3): 541553. DOI: https://doi.org/10.1093/aob/mcu194.
  • Song, J., Feng, G.U., Tian, C. & Zhang, F. (2005). Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Ann Bot 96(3): 399405. DOI: https://doi.org/10.1093/aob/mci196.
  • Song, J., Feng, G., Li, Z.K., Chen, A.D., Chen, X.M. & Zhang, F.S. (2007). Effects of salinity and scarifying seed coat on ion content of embryos and seed germination for Suaeda physophora and Haloxylon ammodendron. Seed Science and Technology 35(3): 615623. DOI: https://doi.org/10.15258/sst.2007.35.3.09.
  • Song, J., Fan, H., Zhao, Y., Jia, Y., Du, X. & Wang, B. (2008). Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquat Bot 88(4): 331337. DOI: https://doi.org/10.1016/j.aquabot.2007.11.004.
  • Song, J., Zhou, J., Zhao, W., Xu, H., Wang, F., Xu, Y., Wang, L. & Tian, C. (2016). Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biol 31(1): 1928. DOI: https://doi.org/10.1111/1442-1984.12071.
  • Song, J., Shi, W., Liu, R., Xu, Y., Sui, N., Zhou, J. & Feng, G. (2017). The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol 32(2): 107114. DOI: https://doi.org/10.1111/1442-1984.12132.
  • Sui, N., Li, M., Li, K., Song, J. & Wang, B.S. (2010). Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48(4): 623629. DOI: https://doi.org/10.1007/s11099-010-0080-x.
  • Sui, N. & Han, G. (2014). Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiol Plant 36(4): 983992. DOI: https://doi.org/10.1007/s11738-013-1477-5.
  • Sui, N., Tian, S., Wang, W., Wang, M. & Fan, H. (2017). Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Front Plant Sci 8: 1337. DOI: https://doi.org/10.3389/fpls.2017.01337.
  • Tada, Y., Kawano, R., Komatsubara, S., Nishimura, H., Katsuhara, M., Ozaki, S., Terashima, S., Yano, K., Endo, C., Sato, M., Okamoto, M., Sawada, Y., Hirai, M.Y. & Kurusu, T. (2019). Functional screening of salt tolerance genes from a halophyte Sporobolus virginicus and transcriptomic and metabolomic analysis of salt tolerant plants expressing glycine-rich RNA-binding protein. Plant Sci 278: 5463. DOI: https://doi.org/0.1016/ j.plantsci.2018.10.019.
  • Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K., Narusaka, Y., Narusaka, M., Zhu, J.K. & Shinozaki, K. (2004). Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135(^):1697–1709. DOI: https://doi.org/10.1104/pp.104.039909.
  • Tanveer, M. & Shah, A.N. (2017). An insight into salt stress tolerance mechanisms of Chenopodium album. Environ Sci Pollut Res 24: 16531–16535. DOI: 10.1007/s11356-017-9337-2.
  • Tuteja, N. (2007). Mechanisms of high salinity tolerance in plants. Methods Enzymol 428: 419438.
  • Wang, H.L., Wang, L., Tian, C.Y. & Huang, Z.Y. (2012). Germination dimorphism in Suaeda acuminata: a new combination of dormancy types for heteromorphic seeds. S Afr J Bot 78: 270275. DOI: https://doi.org/10.1016/j.sajb.2011.05.012.
  • Wang, F., Xu, Y.G., Wang, S., Shi, W., Liu, R., Feng, G. & Song, J. (2015). Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol Biochem 95: 4148. DOI: https://doi.org/10.1016/j.plaphy.2015.07.005.
  • Wang, F.X., Yin, C.H., Song, Y.P., Li, Q., Tian, C.Y. & Song, J. (2018). Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions. Plant Biosyst - Int J Dealing Aspects Plant Biosyst 152(4): 749758. DOI: https://doi.org/10.1080/ 11263504.2017.1330776.
  • Xu, Y., Zhao, Y., Duan, H., Sui, N., Yuan, F. & Song, J. (2017). Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa. BMC Genomics 18(1), 114. DOI: https://doi.org/10.1186/s12864-017-4104-9.
  • Yan, C., Wei, Y. & Yang, M. (2011). Comparative germination of Tamarix ramosissima spring and summer seeds. EXCLI journal 10: 198.
  • Yuan, K., Rashotte, A.M., & Wysocka-Diller, J.W. (2011). ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiol Plant 33(2): 261271. DOI: https://doi.org/10.1007/s11738-010-0542-6.
  • Yuan, F., Guo, J., Shabala, S. & Wang, B. (2019). Reproductive physiology of halophytes: current standing. Front Plant Sci 9: 1954. DOI: https://doi.org/10.3389/fpls.2018.01954.
  • Zhang, H., Zhang, G., Lü, X., Zhou, D. & Han, X. (2015). Salt tolerance during seed germination and early seedling stages of 12 halophytes. Plant Soil 388(1): 229241. DOI: https://doi.org/10.1007/s11104-014-2322-3.
  • Zhang, H., Zhu, J., Gong, Z. & Zhu, J. K. (2022). Abiotic stress responses in plants. Nat Rev Genet 23(2): 104119. DOI: https://doi.org/10.1038/s41576-021-00413-0.
  • Zhang, S., Song, J., Wang, H. & Feng, G. (2010). Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia. J Plant Ecol 3(4): 259267. DOI: https://doi.org/10.1093/jpe/rtq005.
  • Zhang, X., Liao, M., Chang, D. & Zhang, F. (2014). Comparative transcriptome analysis of the Asteraceae halophyte Karelinia caspica under salt stress. BMC Res Notes 7(1): 927. DOI: https://doi.org/10.1186/1756-0500-7-927.
  • Zhao, Y., Yang, Y., Song, Y., Li, Q. & Song, J. (2018). Analysis of storage compounds and inorganic ions in dimorphic seeds of euhalophyte Suaeda salsa. Plant Physiol Biochem 130: 511516. DOI: https://doi.org/10.1016/j.plaphy.2018.08.003.
  • Zhou, C., Sun, Y., Ma, Z. & Wang, J. (2015). Heterologous expression of EsSPDS1 in tobacco plants improves drought tolerance with efficient reactive oxygen species scavenging systems. S Afr J Bot 96: 1928. DOI: https://doi.org/10.1016/j.sajb.2014.10.008.
  • Zhou, J.C., Fu, T.T., Sui, N., Guo, J.R., Feng, G., Fan, J.L. & Song, J. (2016). The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst - Int J Dealing Aspects Plant Biosyst 150(1): 8390. DOI: https://doi.org/10.1080/11263504.2014.976294.
There are 81 citations in total.

Details

Primary Language Turkish
Subjects Botany (Other), Structural Biology, Ecology
Journal Section Review
Authors

Alper Durmaz 0000-0001-6927-3283

Hasan Korkmaz 0000-0002-0011-1590

Mehtap Boyraz 0000-0001-7951-9101

Publication Date June 15, 2023
Published in Issue Year 2023 Volume: 4 Issue: 1

Cite

APA Durmaz, A., Korkmaz, H., & Boyraz, M. (2023). Halofitik Tohumlarda Adaptasyonlar. Türler Ve Habitatlar, 4(1), 60-78. https://doi.org/10.53803/turvehab.1215056
AMA Durmaz A, Korkmaz H, Boyraz M. Halofitik Tohumlarda Adaptasyonlar. turvehab. June 2023;4(1):60-78. doi:10.53803/turvehab.1215056
Chicago Durmaz, Alper, Hasan Korkmaz, and Mehtap Boyraz. “Halofitik Tohumlarda Adaptasyonlar”. Türler Ve Habitatlar 4, no. 1 (June 2023): 60-78. https://doi.org/10.53803/turvehab.1215056.
EndNote Durmaz A, Korkmaz H, Boyraz M (June 1, 2023) Halofitik Tohumlarda Adaptasyonlar. Türler ve Habitatlar 4 1 60–78.
IEEE A. Durmaz, H. Korkmaz, and M. Boyraz, “Halofitik Tohumlarda Adaptasyonlar”, turvehab, vol. 4, no. 1, pp. 60–78, 2023, doi: 10.53803/turvehab.1215056.
ISNAD Durmaz, Alper et al. “Halofitik Tohumlarda Adaptasyonlar”. Türler ve Habitatlar 4/1 (June 2023), 60-78. https://doi.org/10.53803/turvehab.1215056.
JAMA Durmaz A, Korkmaz H, Boyraz M. Halofitik Tohumlarda Adaptasyonlar. turvehab. 2023;4:60–78.
MLA Durmaz, Alper et al. “Halofitik Tohumlarda Adaptasyonlar”. Türler Ve Habitatlar, vol. 4, no. 1, 2023, pp. 60-78, doi:10.53803/turvehab.1215056.
Vancouver Durmaz A, Korkmaz H, Boyraz M. Halofitik Tohumlarda Adaptasyonlar. turvehab. 2023;4(1):60-78.
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