Abstract
Small heat-shock proteins (sHSPs/HSP20s) are closely related to algae and plant thermotolerance, but studies on HSP20 family in Neoporphyra haitanensis are scarce. In this study, a total of eight HSP20 members were identified from the genome of N. haitanensis. It was predicted that most of them encode acidic hydrophilic proteins, locating in various organelles as chloroplasts and endoplasmic reticulum. Phylogenetically, the HSP20 genes of N. haitanensis were closely related to that of other species of Porphyra sensu lato, which evolved independently from that of land plants. In addition, their promoter regions contain a large number of cis-acting elements related to stress response. Based on the expression analysis of six HSP20 genes, it showed that the expression patterns of these genes were different among three conditions of dehydration, heat stress and co-stresses of heat and dehydration, with some genes being very sensitive to heat stress. These results initially indicated that HSP20 genes in N. haitanensis could specifically response to heat stress under gene expression level, suggesting their involvement in the process of thermotolerance of N. haitanensis, which is valuable for further studies on the molecular function of HSP20s in N. haitanensis.
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Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117
Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N, Ball S, Weber APM, Arias MC, Henrissat B, Coutinho PM, Krishnan A, Zäuner S, Morath S, Hilliou F, Egizi A, Perrineau M-M, Yoon HS (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941
Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37
Brawley SH, Blouin NA, Ficko-Blean E, Wheeler GL, Lohr M, Goodson HV, Jenkins JW, Blaby-Haas CE, Helliwell KE, Chan CX, Marriage TN, Bhattacharya D, Klein AS, Badis Y, Brodie J, Cao Y, Collén J, Dittami SM, Gachon CMM, Green BR, Karpowicz SJ, Kim JW, Kudahl UJ, Lin S, Michel G, Mittag M, Olson BJSC, Pangilinan JL, Peng Y, Qiu H, Shu S, Singer JT, Smith AG, Sprecher BN, Wagner V, Wang W, Wang Z-Y, Yan J, Yarish C, Zäuner-Riek S, Zhuang Y, Zou Y, Lindquist EA, Grimwood J, Barry KW, Rokhsar DS, Schmutz J, Stiller JW, Grossman AR, Prochnik SE (2017) Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci USA 114:E6361–E6370
Cao M, Xu KP, Yu XZ, Bi GQ, Liu Y, Kong FN, Sun PP, Tang XH, Du GY, Ge Y, Wang DM, Mao YX (2020) A chromosome-level genome assembly of Pyropia haitanensis (Bangiales, Rhodophyta). Mol Ecol Resour 20:216–227
Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved “alpha-crystallin domain.” J Mol Evol 40:238–248
Chang J, Shi JZ, Lin JZ, Ji DH, Xu Y, Chen CS, Wang WL, **e CT (2021) Molecular mechanism underlying Pyropia haitanensis PhHSP22-mediated increase in the high-temperature tolerance of Chlamydomonas reinhardtii. J Appl Phycol 33:1137–1148
Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, **a R (2020) TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202
Chen YT, Xu Y, Ji DH, Chen CS, **e CT (2015) Cloning and expression analysis of two small heat shock protein (sHsp) genes from Pyropia haitanensis. J Fish China 39:182–192 (in Chinese with English abstract)
Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury JM, Barbosa-Neto JF, Bothwell JH, Bouget FY, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock JM, Coelho SM, Colleoni C, Czjzek M, Silva CD, Delage L, Denoeud F, Ph, (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110:5247–5252
Ding HC, Fei QJ, Zhang P, Wang T, Yan XH (2020) Isolation and characterization of a heat-resistant strain with high yield of Pyropia haitanensis induced by Ultraviolet ray. Aquaculture 521:735050
He YJ, Fan M, Sun YY, Li LL (2018) Genome-wide analysis of watermelon HSP20s and their expression profiles and subcellular locations under stresses. Int J Mol Sci 20:12
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 Synechocystis PCC 6803: Identification of hsp17 as a “fluidity gene.” Proc Natl Acad Sci USA 95:3513–3518
Hsieh MH, Chen JT, **n TL, Chen YM, Lin CY (1992) A class of soybean low molecular weight heat shock proteins immunological study and quantitation. Plant Physiol 99:1279–1284
Hu XL, Li YH, Li CH, Yang HR, Wang W, Lu MH (2010) Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress. J Plant Growth Regul 29:455–464
Huang LB, Peng LN, Yan XH (2021) Multi-omics responses of red algae Pyropia haitanensis to intertidal desiccation during low tides. Algal Res 58:102376
** Y, Yang S, Im S, Jeong WJ, Choi DW (2017) Small heat shock protein, Ptshsp19.3 from marine red algae, Pyropia tenera (Bangiales, Rhodophyta) enhances abiotic stress tolerance in Chlamydomonas. J Plant Biotechnol 44:287–295
Lee JM, Yang EC, Graf L, Yang JH, Qiu H, Zel ZU, Chan CX, Stephens TG, Weber APM, Boo GH, Boo SM, Kim KM, Shin Y, Jung M, Lee SJ, Yim HS, Lee JH, Bhattacharya D, Yoon HS (2018) Analysis of the draft genome of the red seaweed Gracilariopsis chorda provides insights into genome size evolution in Rhodophyta. Mol Biol Evol 35:1869–1886
Li B, Chen CS, Xu Y, Ji D, ** genes as internal controls for studying the gene expression in Pyropia haitanensis(Bangiales, Rhodophyta) by quantitative real-time PCR. Acta Oceanol Sin 33:152–159
Li J, Liu XH (2019) Genome-wide identification and expression profile analysis of the HSP20 gene family in Barley (Hordeum vulgare L.). Peer J 7:e6832
Lopes-Caitar VS, de Carvalho MC, Darben LM, Kuwahara MK, Nepomuceno AL, Dias WP, Abdelnoor RV, Marcelino-Guimarães FC (2013) Genome-wide analysis of the HSP20 gene family in soybean: comprehensive sequence, genomic organization and expression profile analysis under abiotic and biotic stresses. BMC Genomics 14:577
Muthusamy SK, Dalal M, Chinnusamy V, Bansal KC (2017) Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. J Plant Physiol 211:100–113
Nakamoto H, Vígh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306
Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838
Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225–237
Song SS, Gao DH, Yan XH (2020) Transcriptomic exploration of genes related to the formation of archeospores in Pyropia yezoensis (Rhodophyta). J Appl Phycol 32:3295–3304
Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH, Vígh L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci USA 99:13504–13509
Uji T, Gondaira Y, Fukuda S, Mizuta H, Saga N (2019) Characterization and expression profiles of small heat shock proteins in the marine red alga Pyropia yezoensis. Cell Stress Chaperones 1:223–233
Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620
Wang DM, Yu XZ, Xu KP, Bi GQ, Cao M, Zelzion E, Fu CX, Sun PP, Liu Y, Kong FN, Du GY, Tang XH, Yang RJ, Wang JH, Tang L, Wang L, Zhao YJ, Ge Y, Zhuang YY, Mo ZL, Chen Y, Gao T, Guan XW, Chen R, Qu WH, Sun B, Bhattacharya D, Mao YX (2020) Pyropia yezoensis genome reveals diverse mechanisms of carbon acquisition in the intertidal environment. Nat Commun 11:4028
Yan XH, Liang ZQ, Song WL, Huang J, Ma P, Aruga Y (2005) Induction and isolation of artificial pigmentation mutants in Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). J Fish China 29:166–172 (in Chinese with English abstract)
Yan XH, Lv F, Liu CJ, Zheng YF (2010) Selection and characterization of a high-temperature tolerant strain of Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). J Appl Phycol 22:511–516
Yang LE, Deng YY, Xu GP, Russel S, Lu QQ, Brodie J (2020) Redefining Pyropia (Bangiales, Rhodophyta): four new genera, resurrection of Porphyrella and description of Calidia pseudolobata sp. nov. from China. J Phycol 56:862–879
Yu JH, Cheng Y, Feng K, Ruan MY, Ye QJ, Wang RQ, Li ZM, Zhou GZ, Yao ZP, Yang YJ, Wan HJ (2016) Genome-wide identification and expression profiling of tomato HSP20 gene family in response to biotic and abiotic stresses. Front Plant Sci 7:1215
Acknowledgements
The authors want to thanks Dr. Dong-Mei Wang (Ocean University of China) for the help on genomic data analysis.
Funding
This work was supported by the National Key Research and Development Program of China [2018YFD0900606]; the Startup Foundation for Young Teachers of Shanghai Ocean University; and the Open Program of Key Laboratory of Cultivation and High-value Utilization of Marine Organisms in Fujian Province [2020fjscq01].
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Peng, LN., Huang, LB., Gui, TY. et al. Identification and expression profiling of HSP20 genes in Neoporphyra haitanensis. J Appl Phycol 34, 1089–1097 (2022). https://doi.org/10.1007/s10811-022-02686-2
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DOI: https://doi.org/10.1007/s10811-022-02686-2