Characterization and expression profiles of small heat shock proteins in the marine red alga Pyropia yezoensis
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Small heat shock proteins (sHSPs) are found in all three domains of life (Bacteria, Archaea, and Eukarya) and play a critical role in protecting organisms from a range of environmental stresses. However, little is known about their physiological functions in red algae. Therefore, we characterized the sHSPs (PysHSPs) in the red macroalga Pyropia yezoensis, which inhabits the upper intertidal zone where it experiences fluctuating stressful environmental conditions on a daily and seasonal basis, and examined their expression profiles at different developmental stages and under varying environmental conditions. We identified five PysHSPs (PysHSP18.8, 19.1, 19.2, 19.5, and 25.8). Real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR) analysis showed that expression of the genes PysHSP18.8, PysHSP19.5, and PysHSP25.8 was repressed at all the developmental stages under normal conditions, whereas PysHSP19.1 and PysHSP19.2 were overexpressed in mature gametophytes and sporophytes. Exposure of the gametophytes to high temperature, oxidative stress, or copper significantly increased the mRNA transcript levels of all the five genes, while exogenous application of the ethylene precursor 1-aminocylopropane-1-carboxylic acid (ACC) significantly increased the expression levels of PysHSP19.2, PysHSP19.5, and PysHSP25.8. These findings will help to further our understanding of the role of PysHSP genes and provide clues about how Pyropia species can adapt to the stressful conditions encountered in the upper intertidal zone during their life cycle.
KeywordsPyropia yezoensis Small heat shock proteins Red algae Abiotic stress Plant growth hormone
We are grateful to Drs. Katsutoshi Arai and Takafumi Fujimoto (Hokkaido University, Japan) for kindly providing LightCycler 480 system. This study was supported by a grant-in-aid for Young Scientists (B) (16K18740 to T.U.) from the Japan Society for the Promotion of Science (JSPS).
- 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, Collen 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, Zauner-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 U S A 114:E6361–E6370CrossRefGoogle Scholar
- Carra S, Alberti S, Arrigo PA, Benesch JL, Benjamin IJ, Boelens W, Bartelt-Kirbach B, Brundel BJJM, Buchner J, Bukau B, Carver JA, Ecroyd H, Emanuelsson C, Finet S, Golenhofen N, Goloubinoff P, Gusev N, Haslbeck M, Hightower LE, Kampinga HH, Klevit RE, Liberek K, McHaourab HS, McMenimen KA, Poletti A, Quinlan R, Strelkov SV, Toth ME, Vierling E, Tanguay RM (2017) The growing world of small heat shock proteins: from structure to functions. Cell Stress Chaperones 22:601–611CrossRefGoogle Scholar
- 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, Da Silva C, Delage L, Denoeud F, Deschamps P, Dittami SM, Gabaldón T, Gachon CM, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez PJ, McLachlan DH, Meslet-Cladiere L, Moustafa A, Nehr Z, Nyvall Collén P, Panaud O, Partensky F, Poulain J, Rensing SA, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 2013:5247–5252CrossRefGoogle Scholar
- Kobayashi Y, Harada N, Nishimura Y, Saito T, Nakamura M, Fujiwara T, Kuroiwa T, Misumi O (2014) Algae sense exact temperatures: small heat shock proteins are expressed at the survival threshold temperature in Cyanidioschyzon merolae and Chlamydomonas reinhardtii. Genome Biol Evol 6:2731–2740CrossRefGoogle Scholar
- Luo Q, Zhu Z, Zhu Z, Yang R, Qian F, Chen H, Yan X (2014) Different responses to heat shock stress revealed heteromorphic adaptation strategy of Pyropia haitanensis (Bangiales, Rhodophyta). PLoS One 9. https://doi.org/10.1371/journal.pone.0094354
- Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, NakayamaI IF, NakajimaK SM, WadaT KS, Inouye K, Gojobori T, Ikeo K (2013) The first symbiont-free genome sequence of marine red alga, susabi-nori (Pyropia yezoensis). PLoS One 8(3):e57122CrossRefGoogle Scholar
- Pasta SY, Raman B, Ramakrishna T, Rao CM (2004) The IXI/V motif in the C-terminal extension of alpha-crystallins: alternative interactions and oligomeric assemblies. Mol Vis 10:655–662Google Scholar
- Rieping M, Schoffl F (1992) Synergistic effect of upstream sequences, CAAT box elements, and HSE sequences for enhanced expression of chimeric heat-shock genes in transgenic tobacco. Mol Gen Genet 231:226–232Google Scholar
- Sahoo D, Tang X, Yarish C (2002) Porphyra—the economic seaweed as a new experimental system. Curr Sci 83:1313–1316Google Scholar
- Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav:1621–1633. https://doi.org/10.4161/psb.22455