Abstract
Calmodulin (CaM) plays an important regulatory role in plant growth and development. In this study, on the basis of previous transcriptomic annotation a homolog of CaM gene (Pc-CaM7) was identified from the red alga Phycocalida chauhanii (previously known as Porphyra chauhanii). It encoded a 151 amino acids protein with 4 EF-hand regions, which was the typical structure of calmodulin family proteins. Evolutionary analysis showed that Pc-CaM7 shared conserved orthologous relationships with CaMs from Neoporphyra haitanensis (formerly Pyropia haitanensis), Porphyra umbilicalis, and Gracilariopsis chorda. During the developmental period of P. chauhanii gametophytic germlings from 25- to 50-day-old, the asexual archeospores were continuedly released from the marginal region of blades, followed by the emergence of spermatangia from 40-day-old germlings. Based on quantitative real-time PCR analysis, it showed that expression trend of Pc-CaM7 was correlated with the rule of archeospores’ formation and release, whereas in N. haitanensis without archeospore characteristic, the expression pattern of the orthologous gene (Pha_00404) was different, which increased and reached a plateau during the same developmental period. These findings suggested that Pc-CaM7 may be involved in the process of archeospores formation and release, which may provide a foundation for understanding the molecular mechanisms of asexual reproduction in Bangiales.
Similar content being viewed by others
References
Anil Kumar C, Panikkar MVN (1995) The species of Porphyra C.A. Agardh from Kerala. Seaweed Res Utiliz 17:151–160
Anil Kumar C, Panikkar MVN (1997) Indian species of Porphyra (Rhodophyceae, Bangiales). Feddes Repert 108:419–423
Bekesiova I, Nap JP, Mlynarova L (1999) Isolation of high quality DNA and RNA from leaves of the carnivorous plant Drosera rotundifolia. Plant Mol Biol Report 17:269–277
Bhattacharya D, Price PC, Chan CX, Qiu H, Rose N, Ball S, Weber APM, Arias MC, Henrissat B, Coutinho PM, Krishnan A, Zauner S, Morath S, Hilliou F, Egizi A, Perrineau MM, Yoon HS (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941–1950
Brawley SH, Blouin NA, Ficko–Blean E (2017) Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci U S A 114:6361–6370
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
Chen SS, Ding HC, Yan XH (2016) Isolation and characterization of an improved strain of Porphyra chauhanii (Bangiales, Rhodophyta) with high–temperature resistance. J Appl Phycol 28:3031–3041
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–Netoh JF, Bothwell JH, Bouget FY, Brillet L, Cabello–Hurtado F, Capella–Gutiérrez S, Charrier B, Cladière L, Cock JM, Coelho SM, Colleonig C, Czjzek M, Silvac CD, Delage L, Denoeud F, Deschamps P, Dittami SM, Gabaldón T, Gachon CMM, 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, Collén PN, Panaud O, Partensky F, Poulainc 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 110:5247–5252
Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–450
Guiry MD, Guiry GM (2021) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on 11 January 2021
Jiang LC, Schlesinger F, Davis CA, Zhang Y, Li R, Salit M, Gingeras T, Oliver B (2011) Synthetic spike–in standards for RNA–Seq experiments. Genome Res 21:1543–1551
Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin–mediated regulation of gene expression in plants. Mol Plant 2:13–21
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higginset DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lee JM, Yang EC, Graf L, Yang JH, Qiu H, Zelzion U, Chan CX, Stphens 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
Santiañez WJE, Wynne MJ (2020) Proposal of Phycocalidia Santiañez & M.J.Wynne nom. nov. to replace Calidia L.-E.Yang & J.Brodie nom. illeg. (Bangiales, Rhodophyta). Not Alg 140:1–3
Song JT, Yan XH (2015) Cytological studies on Pyropia chauhanii from India. J Fish China 39:1479–1486
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
Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi HG, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols–Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: Generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151
Takahashi M, Saga N, Mikami K (2010) Photosynthesis–dependent extracellular Ca2+ influx triggers an asexual reproductive cycle in the marine red macroalga Porphyra yezoensis. Am J Plant Sci 1:1–11
Tseng CK, Chang TJ (1954) Studies on Porphyra I. Life history of Porphyra tenera Kjellm. Acta Bot Sin 3:287–302
Valentina LV, Paola D, Alessandra A (2018) Towards understanding plant calcium signaling through calmodulin–like proteins: a biochemical and structural perspective. Int J Mol Sci 19:1331–1348
Wang MQ, Mao YX, Zhuang YY, Kong FN, Sui ZH (2009) Cloning and analysis of calmodulin gene from Porphyra yezoensis Ueda (Bangiales, Rhodophyta). J Ocean Univ China 8:247–253
Xu HX, Heath MC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore–serived infection of the cowpea rust fungus. Plant Cell 10:585–597
Yan XH, Fujita Y, Aruga Y (2004) High monospore producing mutants obtained by treatment with MNNG in Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Hydrobiologia 512:133–140
Yang XW, Ding HC, Yan XH (2019) Genetic analysis on the period of meiosis and morphogenesis in gametophytic blades of Pyropia suborbiculata (Bangiales, Rhodophyta). Oceanol Limnol Sin 50:173–180
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 56:1–18
Zhao CY (2016) Cloning and prokaryotic expression and function analysis of PyCaM and PyHSP70 gene from Porphyra yezoensis. Dissertation, Liaoning Normal University
Zheng HY, Wang WL, Xu K, Xu Y, Ji DH, Chen CS (2020) Ca2+ influences heat shock signal transduction in Pyropia haitanensis. Aquaculture 516:1–8
Acknowledgements
The authors would also like to thank Profs Michael Guiry and Michael Borowitzka for their assistance in resolving the nomenclatural status of this species.
Funding
This research is supported by the National Key Research and Development Program of China (2018YFD09006); The Initial Funding for Young Scholars of Shanghai Ocean University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 213 kb)
Rights and permissions
About this article
Cite this article
Li, H., Gao, D. & Yan, X. Identification and expression analysis of a calmodulin gene in Phycocalida chauhanii (Rhodophyceae, Bangiales). J Appl Phycol 33, 1915–1923 (2021). https://doi.org/10.1007/s10811-021-02405-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-021-02405-3