Heat-stress Memory is Responsible for Acquired Thermotolerance in Bangia fuscopurpurea.
Journal
Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
received:
27
03
2019
accepted:
18
06
2019
pubmed:
25
6
2019
medline:
10
5
2020
entrez:
25
6
2019
Statut:
ppublish
Résumé
The environmental stresses that sessile organisms experience usually fluctuate dramatically and are often recurrent. Terrestrial plants can acquire memory of exposure to sublethal heat stress to acquire thermotolerance and survive subsequent lethal high-temperature stress; however, little is known concerning whether seaweeds acquire thermotolerance via heat-stress memory. We have demonstrated that the red seaweed Bangia fuscopurpurea can indeed acquire memory of sublethal high-temperature stress, resulting in the acquisition of thermotolerance that protects against subsequent lethal high-temperature stress. Moreover, the maintenance of heat-stress memory was associated with a slight increase in the saturation level of membrane fatty acids. This suggests that the modification of membrane fluidity via changes in membrane fatty acid composition is involved in the establishment and maintenance of heat-stress memory in B. fuscopurpurea. These findings provide insights into the physiological survival and growth strategies of sessile red seaweeds to cope with recurrent changes in environmental conditions.
Substances chimiques
Fatty Acids
0
Types de publication
Letter
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
971-975Informations de copyright
© 2019 Phycological Society of America.
Références
Barnabás, B., Jäger, K. & Fehér, A. 2008. The effect of drought and heat stress on reproductive process in cereals. Plant, Cell Environ. 31:11-38.
Bäurle, I. 2016. Plant heat adaptation: priming in response to heat stress. F1000Res. 5:694.
Blouin, N. A., Brodie, J. A., Grossman, A. C., Xu, P. & Brawley, S. H. 2011. Porphyra: a marine crop shaped by stress. Trends Plant Sci. 16:29-37.
Bruce, T. J. A., Matthes, M. C., Napier, J. A. & Pickett, J. A. 2007. Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci. 173:603-8.
Cao, M., Wang, D., Mao, Y., Kong, F., Bi, G., Xing, Q. & Weng, Z. 2017. Integrating transcriptomics and metabolomics to characterize the regulation of EPA biosynthesis in response to Cold stress in seaweed Bangia fuscopurpurea. PLoS ONE 12:e0186986.
Carratù, L., Franceschelli, S., Pardini, C. L., Kobayashi, G. S., Horvath, I., Vigh, L. & Maresca, B. 1996. Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc. Natl. Acad. Sci. USA 93:3870-5.
Choi, S., Hwang, M. S., Im, S., Kim, N., Jeong, W. J., Park, E. J. & Gong, Y. G. 2013. Transcriptome sequencing and comparative analysis of the gametophyte thalli of Pyropia tenera under normal and high temperature conditions. J. Appl. Phycol. 25:1237-46.
Cramer, G. R., Urano, K., Delrot, S., Pezzotti, M. & Shinozaki, K. 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11:163.
Crisp, P. A., Ganguly, D., Eichten, S. R., Borevitz, J. O. & Pogson, B. J. 2016. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2:e1501340.
Ding, H., Zhang, B. & Yan, X. 2016. Isolation and characterization of a heat-resistant strain with high yield of Pyropia yezoensis Ueda (Bangiales, Rhodophyta). Aquac. Fish. 1:24-33.
Friedrich, T., Faivre, L., Bäurle, I. & Schubert, D. 2019. Chromatin-based mechanisms of temperature memory in plants. Plant, Cell Environ. 42:762-70.
Hatfield, J. L. & Prueger, J. H. 2015. Temperature extremes: effect on plant growth and development. Weather Clim. Extrem. 10:4-10.
Horváth, I., Glatz, A., Varvasovszki, V., Török, Z., Páli, T., Balogh, G., Kovács, E., Nádasdi, L., Benkö, S., Joó, F. & Vígh, L. 1998. Membrane physical state controls the signaling mechanism of the heat shock response in Synechcoystis PCC 6803: identification of hsp17 as a “fluidity gene”. Proc. Natl. Acad. Sci. USA 95:3513-8.
Im, S., Choi, S., Hwang, M. S., Park, E. J. & Choi, D. W. 2015. De novo assembly of transcriptome from the gametophyte of the marine red algae Pyropia seriata and identification of abiotic stress response genes. J. Appl. Phycol. 27:1343-53.
Königshofer, H., Tromballa, H. W. & Löppert, H. G. 2008. Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant, Cell Environ. 31:1771-80.
Kumar, A. A., Mishra, P., Kumari, K. & Panigrahi, K. C. 2012. Environmental stress influencing plant development and flowering. Front. Biosci. (Schol Ed) 4:1315-24.
Kusch, T., Mei, A. & Nguyen, C. 2014. Histone H3 lysine 4 trimethylation regulates cotranscriptional H2A variant exchange by Tip60 complexes to maximize gene expression. Proc. Natl. Acad. Sci. USA 111:4850-5.
Lämke, J. & Bäurle, I. 2017. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 18:124.
Lämke, J., Brzezinka, K., Altmann, S. & Bäurle, I. 2016. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 35:162-75.
Leach, M. D. & Cowen, L. E. 2014. Membrane fluidity and temperature sensing are coupled via circuitry comprised of Ole1, Rsp5, and Hsf1 in Candida albicans. Eukaryot. Cell 13:1077-84.
Lee, H. J., Park, E. J. & Choi, J. I. 2019. Isolation, morphological characteristics and proteomic profile analysis of thermo-tolerant Pyropia yezoensis mutant in response to high-temperature stress. Ocean Sci. J. 54:65-78.
Liu, H. C., Lämke, J., Lin, S. Y., Hung, M. J., Liu, K. M., Charng, Y. Y. & Bäurle, I. 2018. Distinct heat shock factors and chromatin modifications mediate the organ-autonomous transcriptional memory of heat stress. Plant J. 95:401-13.
Mikami, K., Ito, M., Taya, K., Kishimoto, I., Kobayashi, T., Itabashi, Y. & Tanaka, R. 2018. Parthenosporophytes of the brown alga Ectocarpus siliculosus exhibit sex-dependent differences in thermotolerance as well as fatty acid and sterol composition. Mar. Environ. Res. 137:188-95.
Mikami, K. & Kishimoto, I. 2018. Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan. Algal Res. 11:25-32.
Mumford, T. F. & Miura, A. 1988. Porphyra as food: cultivation and economics. In Lembi, C. A. & Waaland, J. R. [eds.] Algae and Human Affairs. Cambridge University Press, London, UK, pp. 87-117.
Murakami, Y., Tsuyama, M., Kobayashi, Y., Kodama, H. & Iba, K. 2000. Trienoic fatty acids and plant tolerance of high temperature. Science 28:476-9.
Notoya, M. & Iijima, N. 2003. Life history and sexuality of archeospore and apogamy of Bangia atropurpurea (Roth) Lyngbye (Bangiales, Rhodophyta) from Fukaura and Enoshima, Japan. Fish. Sci. 69:799-805.
Pandey, P., Irulappan, V., Bagavathiannan, M. V. & Senthil-Kumar, M. 2017. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front. Plant Sci. 8:537.
Sangwan, V., Örvar, B. L., Beyerly, J., Hirt, H. & Dhindsa, R. S. 2002. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31:629-38.
Sanyal, R. P., Misra, H. S. & Saini, A. 2018. Heat-stress priming and alternative splicing-linked memory. J. Exp. Bot. 69:2431-4.
Sommerfeld, M. A. & Nichols, H. W. 1973. The life cycle of Bangia fuscopurpurea in culture. I. Effects of temperature and photoperiod on the morphology and reproduction of the Bangia phase. J. Phycol. 9:205-10.
Sun, P., Mao, Y., Li, G., Cao, M., Kong, F., Wang, L. & Bi, G. 2015. Comparative transcriptome profiling of Pyropia yezoensis (Ueda) M.S. Hwang & H.G. Choi in response to temperature stresses. BMC Genom. 16:463.
Wang, W., Chang, J., Zheng, H., Ji, D., Xu, Y., Chen, C. & Xie, C. 2018b. Full-length transcriptome sequences obtained by a combination of sequencing platforms applied to heat shock proteins and polyunsaturated fatty acids biosynthesis in Pyropia haitanensis. J. Appl. Phycol. 31:1483-92.
Wang, W., Teng, F., Lin, Y., Ji, D., Xu, Y., Chen, C. & Xie, C. 2018a. Transcriptomic study to understand thermal adaptation in a high temperature-tolerant strain of Pyropia haitanensis. PLoS ONE 13:e0195842.
Wang, W. J., Zhu, J. Y., Xu, P., Xu, J. R., Lin, X. Z., Huang, C. K., Song, W. L., Peng, G. & Wang, G. C. 2008. Characterization of the life history of Bangia fuscopurpurea (Bangiaceae, Rhodophyta) in connection with its cultivation in China. Aquaculture 278:101-9.
Yan, X. H., Lv, F., Liu, C. J. & Zheng, Y. F. 2010. Selection and characterization of a high-temperature tolerant strain of Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). J. Appl. Phycol. 22:511-6.
Zinn, K. E., Tunc-Ozdemir, M. & Harper, J. F. 2010. Temperature stress and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61:1959-68.