Skip to main content

Advertisement

Springer Nature Link
Log in

Transcriptomic analysis under ethylene precursor treatment uncovers the regulation of gene expression linked to sexual reproduction in the dioecious red alga Pyropia pseudolinearis

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The marine red algal genus Pyropia, class Bangiophyceae, includes dioecious and monoecious species; however, the molecular mechanisms underlying control of their sexual reproduction are still poorly understood. In the present study, we demonstrated that application of the ethylene precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), promoted the formation of spermatangia and parthenosporangia in male and female gametophytes, respectively, of the dioecious species Pyropia pseudolinearis. In addition, we determined expression profiles of ACC-responsive genes in the gametophytes during sexual reproduction using RNA-Seq and quantitative real-time PCR (qRT-PCR). Genes involved in the regulation of cell division and cell wall organization, such as high-mobility group (PpHMG) and glycosyltransferase family (PpGT14), were found to be upregulated in male and female gametophytes treated with ACC. In addition, the relatively rapid ACC-response of the vesicular-trafficking-related genes, flotillin (PpFLOT), charged multivesicular body protein 5 (PpCHMP5), and peptidase family S8 (PpS8) was shown to occur during male and female sexual reproduction. Expression levels of these six genes in the monoecious species P. yezoensis, which are homologs to ACC-responsive genes in P. pseudolinearis, also increased in gametophytes treated with ACC. These findings could provide new insights into the ACC-regulation of the sexual life cycle in Pyropia species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Adoro S, Park KH, Bettigole SE, Lis R, Shin HR, Seo H, Kim JH, Knobeloch KP, Shim JH, Glimcher LH (2017) Post-translational control of T cell development by the ESCRT protein CHMP5. Nat Immunol 18:780–790

    Article  CAS  PubMed  Google Scholar 

  • Antosch M, Mortensen SA, Grasser KD (2012) Plant proteins containing high mobility group box DNA-binding domains modulate different nuclear processes. Plant Physiol 159:875–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antosch M, Schubert V, Holzinger P, Houben A, Grasser KD (2015) Mitotic lifecycle of chromosomal 3xHMG-box proteins and the role of their N-terminal domain in the association with rDNA loci and proteolysis. New Phytol 208:1067–1077

    Article  CAS  PubMed  Google Scholar 

  • Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandstadter J, Rossbach C, Theres K (1994) The pattern of histone H4 expression in the tomato shoot apex changes during development. Planta 192:69–74

    CAS  PubMed  Google Scholar 

  • 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–E6370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404

    Article  Google Scholar 

  • Chamberlain AHL, Evans LV (1973) Aspects of spore production in the red alga Ceramium. Protoplasma 76:139–159

    Article  Google Scholar 

  • Cole K, Sheath RG (1980) Ultrastructural changes in major organelles during spermatial differentiation in Bangia (Rhodophyta). Protoplasma 102:253–279

    Article  Google Scholar 

  • Cole KM, Park CM, Reid PE, Sheath RG (1985) Comparative studies on the cell walls of sexual and asexual Bangia atropurpurea (Rhodophyta) .I. Histochemistry of polysaccharides. J Phycol 21:585–592

    Article  Google Scholar 

  • Cortes F, Pastor N, Mateos S, Dominguez I (2003) Roles of DNA topoisomerases in chromosome segregation and mitosis. Mutat Res Rev Mutat 543:59–66

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2000) loosening of plant cell walls by expansins. Nature 407:321–326

    Article  CAS  PubMed  Google Scholar 

  • de Gassart A, Geminard C, Fevrier B, Raposo G, Vidal M (2003) Lipid raft-associated protein sorting in exosomes. Blood 102:4336–4344

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Jimenez P, Robaina RR (2015) On reproduction in red algae: further research needed at the molecular level. Front Plant Sci 6:93

    PubMed  PubMed Central  Google Scholar 

  • Garcia-Jimenez P, Brito-Romano O, Robaina RR (2016) Occurrence of jasmonates during cystocarp development in the red alga Grateloupia imbricata. J Phycol 52:1085–1093

    Article  CAS  Google Scholar 

  • Garcia-Jimenez P, Montero-Fernández M, Robaina RR (2017) Molecular mechanisms underlying Grateloupia imbricata (Rhodophyta) carposporogenesis induced by methyl jasmonate. J Phycol 53:1340–1344

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Jimenez P, Montero-Fernández M, Robaina RR (2018) Analysis of ethylene-induced gene regulation during carposporogenesis in the red seaweed Grateloupia imbricata (Rhodophyta). J Phycol 54:681–689

    Article  CAS  PubMed  Google Scholar 

  • Guzman-Urióstegui A, García-Jiménez P, Marián F, Robledo D, Robaina R (2002) Polyamines influence maturation in reproductive structures of Gracilaria cornea (Gracilariales, Rhodophyta). J Phycol 38:1169–1175

    Article  Google Scholar 

  • Guzman-Urióstegui A, Robaina RR, Freile-Pelegri Y, Robledo D (2012) Polyamines increase carpospore output and growth during in vitro cultivation of Hydropuntia cornea. Biotechnol Lett 34:755–761

    Article  CAS  PubMed  Google Scholar 

  • Har-Vardi I, Mali R, Breietman M, Sonin Y, Albotiano S, Levitas E, Potashnik G, Priel E (2007) DNA topoisomerases I and II in human mature sperm cells: characterization and unique properties. Hum Reprod 22:2183–2189

    Article  CAS  PubMed  Google Scholar 

  • Hawkes MW (1990) Reproductive strategies. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, Cambridge, pp 455–476

    Google Scholar 

  • Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75:193–208

    Article  CAS  PubMed  Google Scholar 

  • Jasencakova Z, Meister A, Walter J, Turner BM, Schubert I (2000) Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12:2087–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapanidou M, Curtis NL, Bolanos-Garcia VM (2017) Cdc20: at the crossroads between chromosome segregation and mitotic exit. Trends Biochem Sci 42:193–205

    Article  CAS  PubMed  Google Scholar 

  • Kevei Z, Baloban M, Da Ines O, Tiricz H, Kroll A, Regulski K, Mergaert P, Kondorosi E (2011) Conserved CDC20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana. PLoS One 6:e20618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim NG (2011) Culture study on the hybrid by interspecific crossing between Porphyra pseudolinearis and P. dentata (Bangiales, Rhodophyta), two dioecious species in culture. Algae 26:79–86

    Article  Google Scholar 

  • Kim SH, Kim GH (1999) Cell-cell recognition during fertilization in the red alga, Aglaothamnion oosumiense (Ceramiaceae, Rhodophyta). Hydrobiologia 399:81–89

    Article  Google Scholar 

  • Lee Y, El Andaloussi S, Wood MJA (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21:R125–R134

    Article  CAS  Google Scholar 

  • Lee J, Yang EC, Graf L, Yang JH, Qiu H, Zelzion U, 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 1:1869–1886

    Article  CAS  Google Scholar 

  • Liu XJ, Bogaert K, Engelen AH, Leliaert F, Roleda MY, De Clerck O (2017) Seaweed reproductive biology: environmental and genetic controls. Bot Mar 60:89–108

    Article  Google Scholar 

  • Marchant R, Robards AW (1968) Membrane systems associated with the plasmalemma of plant cells. Ann Bot 32:457–471

    Article  Google Scholar 

  • Meshi T, Taoka K, Iwabuchi M (2000) Regulation of histone gene expression during the cell cycle. Plant Mol Biol 43:643–657

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki JH, Yang SF (1987) Metabolism of 5-methylthioribose to methionine. Plant Physiol 84:277–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K (2013) The first symbiont-free genome sequence of marine red alga, susabi-nori (Pyropia yezoensis). PLoS One 8:e57122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neefus CD, Mathieson AC, Bray TL, Yarish C (2008) The distribution, morphology, and ecology of three introduced asiatic species of Porphyra (Bangiales, Rhodophyta) in the northwestern Atlantic. J Phycol 44:1399–1414

    Article  PubMed  Google Scholar 

  • Otto GP, Nichols BJ (2011) The roles of flotillin microdomains-endocytosis and beyond. J Cell Sci 124:3933–3940

    Article  CAS  PubMed  Google Scholar 

  • Ouriques LC, Schmidt EC, Bouzon ZL (2012) The mechanism of adhesion and germination in the carpospores of Porphyra spiralis var. amplifolia (Rhodophyta, Bangiales). Micron 43:269–277

    Article  CAS  PubMed  Google Scholar 

  • Pedersen DS, Coppens F, Ma L, Antosch M, Marktl B, Merkle T, Beemster GTS, Houben A, Grasser KD (2011) The plant-specific family of DNA-binding proteins containing three HMG-box domains interacts with mitotic and meiotic chromosomes. New Phytol 192:577–589

    Article  CAS  PubMed  Google Scholar 

  • Peel S, Macheboeuf P, Martinelli N, Weissenhorn W (2011) Divergent pathways lead to ESCRT-III-catalyzed membrane fission. Trends Biochem Sci 36:199–210

    Article  CAS  PubMed  Google Scholar 

  • Phuyal S, Hessvik NP, Skotland T, Sandvig K, Llorente A (2014) Regulation of exosome release by glycosphingolipids and flotillins. FEBS J 281:2214–2227

    Article  CAS  PubMed  Google Scholar 

  • Potapova T, Gorbsky GJ (2017) The consequences of chromosome segregation errors in mitosis and meiosis. Biology (Basel) 6:E12

    Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Culture and collections of algae, Proc US-Japan Conf, Hakone, September 1966. Jpn Soc Plant Physiol Tokyo, pp 63–75

  • Rawlings ND, Waller M, Barrett AJ, Bateman A (2014) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 42:D503–D509

    Article  CAS  PubMed  Google Scholar 

  • Sacramento AT, García-Jiménez P, Alcázar R, Tiburcio AF, Robaina RR (2004) Influence of polyamines on the sporulation of Grateloupia (Halymeniaceae, Rhodophyta). J Phycol 40:887–894

    Article  CAS  Google Scholar 

  • Shim E, Shim J, Klochkova TA, Han JW, Kim GH (2012) Purification of a sex-specific lectin involved in gamete binding of Aglaothamnion callophyllidicola (Rhodophyta). J Phycol 48:916–924

    Article  CAS  PubMed  Google Scholar 

  • Stros M, Launholt D, Grasser KD (2007) The HMG-box: a versatile protein domain occurring in a wide variety of DNA-binding proteins. Cell Mol Life Sci 64:2590–2606

    Article  CAS  PubMed  Google Scholar 

  • Taylor AA, Horsch A, Rzepczyk A, Hasenkampf CA, Riggs CD (1997) Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis. Plant J 12:1261–1271

    Article  CAS  PubMed  Google Scholar 

  • Toyooka K, Goto Y, Asatsuma S, Koizumi M, Mitsui T, Matsuoka K (2009) A mobile secretory vesicle cluster involved in mass transport from the Golgi to the plant cell exterior. Plant Cell 21:1212–1229

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsekos I, Schnepf E (1991) Acid phosphatase activity during spore differentiation of the red algae Gigartina teedii and Chondria tenuissima. Plant Syst Evol 176:35–51

    Article  CAS  Google Scholar 

  • Uji T, Monma R, Mizuta H, Saga N (2012) Molecular characterization and expression analysis of two Na+/H+ antiporter genes in the marine red alga Porphyra yezoensis. Fish Sci 78:985–991

    Article  CAS  Google Scholar 

  • Uji T, Matsuda R, Takechi K, Takano H, Mizuta H, Takio S (2016) Ethylene regulation of sexual reproduction in the marine red alga Pyropia yezoensis (Rhodophyta). J Appl Phycol 28:3501–3509

    Article  CAS  Google Scholar 

  • Xie SP, Lam E (1994) Abundance of nuclear-DNA topoisomerase-II is correlated with proliferation in Arabidopsis thaliana. Nucleic Acids Res 22:5729–5736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Drs. Katsutoshi Arai and Takafumi Fujimoto (Hokkaido University, Japan) for kindly providing the CLC Genomics Workbench. This study was supported by grant-in-aid for the Young Scientists (B) (16 K18740 to T.U.) from the Japan Society for the Promotion of Science (JSPS), and grant-in-aid from the Akiyama Life Science Foundation (T.U.).

Author information

Authors and Affiliations

  1. Division of Marine Life Science, Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Ryo Yanagisawa, Naoki Sekine, Hiroyuki Mizuta & Toshiki Uji

Authors
  1. Ryo Yanagisawa
    View author publications

    Search author on:PubMed Google Scholar

  2. Naoki Sekine
    View author publications

    Search author on:PubMed Google Scholar

  3. Hiroyuki Mizuta
    View author publications

    Search author on:PubMed Google Scholar

  4. Toshiki Uji
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Toshiki Uji.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 650 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yanagisawa, R., Sekine, N., Mizuta, H. et al. Transcriptomic analysis under ethylene precursor treatment uncovers the regulation of gene expression linked to sexual reproduction in the dioecious red alga Pyropia pseudolinearis. J Appl Phycol 31, 3317–3329 (2019). https://doi.org/10.1007/s10811-019-01808-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01808-7

Keywords

Profiles

  1. Toshiki Uji View author profile