Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima

English version

Autoři: Gareth A. Pearson ^aff001; Neusa Martins ^aff001; Pedro Madeira ^aff001; Ester A. Serrão ^aff001; Inka Bartsch ^aff002
Působiště autorů: Centre for Marine Sciences (CCMAR)-CIMAR, University of Algarve, Portugal ^aff001; Alfred-Wegener-Institute, Helmholtz Center for Polar and Marine Research, Am Handelshafen, Germany ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0219723

Souhrn

In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.

Klíčová slova:

Biology and life sciences – Cell biology – Genetics – Gene expression – Genomics – Genome analysis – Biochemistry – Organisms – Eukaryota – Plants – Computational biology – Proteins – DNA-binding proteins – Medicine and health sciences – Physiology – Reproductive physiology – Protein domains – Algae – Transcriptome analysis – Gametogenesis – Motor proteins – Molecular motors – Seaweed

Zdroje

1. van Werven FJ, Amon A. Regulation of entry into gametogenesis. Philos Trans R Soc B Biol Sci. 2011;366(1584):3521–31.

2. Richerd S, Couvet D, Valéro M. Evolution of the alternation of haploid and diploid phases in life cycles. II. Maintenance of the haplo‐diplontic cycle. J Evol Biol. 1993;6(2):263–80.

3. Mable BK, Otto SP. The evolution of life cycles with haploid and diploid phases. Vol. 20, BioEssays. John Wiley & Sons, Inc; 1998.

4. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature. 2010 Jun;465(7298):617–21. doi: 10.1038/nature09016 20520714

5. Garbary DJ, Kim KY, Klinger T, Duggins D. Red algae as hosts for endophytic kelp gametophytes. Mar Biol. 1999 Oct;135(1):35–40.

6. Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, et al. The genus Laminaria sensu lato: Recent insights and developments. Eur J Phycol. 2008;43(1):1–86.

7. Martins N, Pearson GA, Gouveia L, Tavares AI, Serrão EA, Bartsch I. Hybrid vigour for thermal tolerance in hybrids between the allopatric kelps Laminaria digitata and L. pallida with contrasting thermal affinities. European Journal of Phycology. 2019; in press.

8. Luning K, Dring MJ. Reproduction, growth and photosynthesis of gametophytes of Laminaria saccharina grown in blue and red light. Mar Biol. 1975;29:195–200.

9. Motomura T, Sakai Y. Ultrastructural studies of gametogenesis in Laminaria angustata (Laminariales, Phaeophyta) regulated by iron concentration in the medium. Phycologia. 1984 Sep 6;23(3):331–43.

10. Müller DG, Gassmann G, Lüning K. Isolation of a spermatozoid-releasing and -attracting substance from female gametophytes of Laminaria digitata. Nature. 1979;279(5712):430–1. doi: 10.1038/279430a0 16068180

11. Müller DG. Relative sexuality in Ectocarpus siliculosus. Arch Microbiol. 1976;109(1–2):89–94.

12. Ahmed S, Cock JM, Pessia E, Luthringer R, Cormier A, Robuchon M, et al. A Haploid System of Sex Determination in the Brown Alga Ectocarpus sp. Curr Biol. 2014 Aug;1–13.

13. Lipinska AP, Toda NRT, Heesch S, Peters AF, Cock JM, Coelho SM. Multiple gene movements into and out of haploid sex chromosomes. Genome Biol. 2017 Dec 8;18(1):104. doi: 10.1186/s13059-017-1201-7 28595587

14. Ye N, Zhang X, Miao M, Fan X, Zheng Y, Xu D, et al. Saccharina genomes provide novel insight into kelp biology. Nat Commun. 2015;6:6986. doi: 10.1038/ncomms7986 25908475

15. Coelho SM, Mignerot L, Cock JM. Origin and evolution of sex-determination systems in the brown algae. New Phytol. 2019;

16. Martins MJF, Mota CF, Pearson GA. Sex-biased gene expression in the brown alga Fucus vesiculosus. BMC Genomics. 2013 Jan;14:294. doi: 10.1186/1471-2164-14-294 23634783

17. Lipinska A, Cormier A, Luthringer R, Peters AF, Corre E, Gachon CMM, et al. Sexual dimorphism and the evolution of sex-biased gene expression in the brown alga Ectocarpus. Mol Biol Evol. 2015;32(6):1581–97. doi: 10.1093/molbev/msv049 25725430

18. Shan TF, Pang SJ, Li J, Li X. De novo transcriptome analysis of the gametophyte of Undaria pinnatifida (Phaeophyceae). J Appl Phycol. 2015;27(2):1011–9.

19. Bartsch I, Vogt J, Pehlke C, Hanelt D. Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea). J Phycol. 2013;49(6):1061–73. doi: 10.1111/jpy.12125 27007627

20. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Chang. 2013 Jan 22;3(1):78–82.

21. Raybaud V, Beaugrand G, Goberville E, Delebecq G, Destombe C, Valero M, et al. Decline in Kelp in West Europe and Climate. Thrush S, editor. PLoS One. 2013 Jun 26;8(6):e66044. doi: 10.1371/journal.pone.0066044 23840397

22. Robuchon M, Le Gall L, Mauger S, Valero M. Contrasting genetic diversity patterns in two sister kelp species co-distributed along the coast of Brittany, France. Mol Ecol. 2014;23(11):2669–85. doi: 10.1111/mec.12774 24787679

23. Hargrave MS, Foggo A, Pessarrodona A, Smale DA. The effects of warming on the ecophysiology of two co-existing kelp species with contrasting distributions. Oecologia. 2017 Feb 23;183(2):531–43. doi: 10.1007/s00442-016-3776-1 27878385

24. Neiva J, Paulino C, Nielsen MM, Krause-Jensen D, Saunders GW, Assis J, et al. Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissima. Sci Rep. 2018 Dec 18;8(1):1112. doi: 10.1038/s41598-018-19620-7 29348650

25. Gerard V a., Du Bois KR. Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina. Mar Biol. 1988 Apr;97(4):575–80.

26. Breton TS, Nettleton JC, O’Connell B, Bertocci M. Fine-scale population genetic structure of sugar kelp, Saccharina latissima (Laminariales, Phaeophyceae), in eastern Maine, USA. Phycologia. 2018 Jan 8;57(1):32–40. doi: 10.2216/17-72.1 29170569

27. Provasoli L. Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A, editors. Cultures and Collections of Algae. Proceedings of the US Japan Conference, Hakone. Japanese Society of Plant Physiology, Tokyo; 1966. p. 63–75.

28. Zhang QS, Qu SC, Cong YZ, Luo SJ, Tang XX. High throughput culture and gametogenesis induction of Laminaria japonica gametophyte clones. J Appl Phycol. 2008;20:205–11.

29. Pearson G, Lago-Leston A, Valente M, Serrão E. Simple and rapid RNA extraction from freeze-dried tissue of brown algae and seagrasses. Eur J Phycol. 2006;41:97–104.

30. Brown CT, Howe A, Zhang Q, Pyrkosz AB, Brom TH. A Reference-Free Algorithm for Computational Normalization of Shotgun Sequencing Data. arXiv. 2012 Mar 21;1–18.

31. Schulz MH, Zerbino DR, Vingron M, Birney E. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics. 2012 Apr 15;28(8):1086–92. doi: 10.1093/bioinformatics/bts094 22368243

32. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015 Jan 17;12(1):59–60. doi: 10.1038/nmeth.3176 25402007

33. Rho M, Tang H, Ye Y. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 2010 Nov;38(20):e191. doi: 10.1093/nar/gkq747 20805240

34. Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016 Oct 18;4:e2584–e2584. doi: 10.7717/peerj.2584 27781170

35. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva E V, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015 Jun 9;31(19):3210–2. doi: 10.1093/bioinformatics/btv351 26059717

36. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011 Jan;12:323. doi: 10.1186/1471-2105-12-323 21816040

37. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012 Apr 4;9(4):357–9. doi: 10.1038/nmeth.1923 22388286

38. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010 Jan 1;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308

39. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015/01/20. 2015 Apr 20;43(7):e47–e47. doi: 10.1093/nar/gkv007 25605792

40. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004 Mar 19;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147

41. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000 Apr;17(4):540–52. doi: 10.1093/oxfordjournals.molbev.a026334 10742046

42. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010 May;59(3):307–21. doi: 10.1093/sysbio/syq010 20525638

43. Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32(18):2847–9. doi: 10.1093/bioinformatics/btw313 27207943

44. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York; 2016.

45. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236–40. doi: 10.1093/bioinformatics/btu031 24451626

46. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000 Jan 1;28(1):27–30. doi: 10.1093/nar/28.1.27 10592173

47. Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters. Omi A J Integr Biol. 2012;16(5):284–7.

48. Coelho SM, Godfroy O, Arun A, Le G, Peters AF, Cock JM. OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. Proc Natl Acad Sci USA. 2011;108(28):11518–23. doi: 10.1073/pnas.1102274108 21709217

49. Arun A, Coelho SM, Peters AF, Bourdareau S, Pérès L, Scornet D, et al. Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae. Elife. 2019;8:1–25.

50. Binda O, Sevilla A, LeRoy G, Lemischka IR, Garcia BA, Richard S. SETD6 monomethylates H2AZ on lysine 7 and is required for the maintenance of embryonic stem cell self-renewal. Epigenetics. 2013 Feb 27;8(2):177–83. doi: 10.4161/epi.23416 23324626

51. Feldman M, Vershinin Z, Goliand I, Elia N, Levy D. The methyltransferase SETD6 regulates Mitotic progression through PLK1 methylation. Proc Natl Acad Sci. 2019 Jan 22;116(4):1235–40. doi: 10.1073/pnas.1804407116 30622182

52. Sanchez CG, Teixeira FK, Czech B, Preall JB, Zamparini AL, Seifert JRK, et al. Regulation of Ribosome Biogenesis and Protein Synthesis Controls Germline Stem Cell Differentiation. Cell Stem Cell. 2016;18(2):276–90. doi: 10.1016/j.stem.2015.11.004 26669894

53. Li H-J, Liu N-Y, Shi D-Q, Liu J, Yang W-C. YAO is a nucleolar WD40-repeat protein critical for embryogenesis and gametogenesis in Arabidopsis. BMC Plant Biol. 2010 Aug;10(1):169.

54. Liu M, Shi D-Q, Yuan L, Liu J, Yang W-C. SLOW WALKER3, Encoding a Putative DEAD-box RNA Helicase, is Essential for Female Gametogenesis in Arabidopsis. J Integr Plant Biol. 2010 Sep 1;52(9):817–28. doi: 10.1111/j.1744-7909.2010.00972.x 20738726

55. Alipanah L, Rohloff J, Winge P, Bones AM, Brembu T. Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum. J Exp Bot. 2015;66(20):6281–96. doi: 10.1093/jxb/erv340 26163699

56. Zehr JP, Falkowski PG. Pathway of ammonium assimilation in a marine diatom determined with the radiotracer 13 N. J Phycol. 1988 Dec;24(4):588–91.

57. Guerra LT, Levitan O, Frada MJ, Sun JS, Falkowski PG, Dismukes GC. Regulatory branch points affecting protein and lipid biosynthesis in the diatom Phaeodactylum tricornutum. Biomass and Bioenergy. 2013 Dec;59:306–15.

58. Maxwell DP, Falk S, Trick CG, Huner NPA. Growth at Low Temperature Mimics High-Light Acclimation in Chlorella vulgaris. Plant Physiol. 1994 Jun;105(2):535–43. doi: 10.1104/pp.105.2.535 12232221

59. Cruz C, Ventura F, Bartrons R, Rosa JL. HERC3 binding to and regulation by ubiquitin. FEBS Lett. 2001 Jan 12;488(1–2):74–80. doi: 10.1016/s0014-5793(00)02371-1 11163799

60. Majumder AL, Johnson MD, Henry SA. 1l-myo-Inositol-1-phosphate synthase. Biochim Biophys Acta—Lipids Lipid Metab. 1997;1348(1):245–56.

61. Smart CC, Fleming AJ. A plant gene with homology to D-myo-inositol-3-phosphate synthase is rapidly and spatially up-regulated during an abscisic-acid-induced morphogenic response in Spirodela polyrrhiza. Plant J. 1993 Aug;4(2):279–93. doi: 10.1046/j.1365-313x.1993.04020279.x 8220483

62. Hegeman CE, Good LL, Grabau EA. Expression of d-myo-Inositol-3-Phosphate Synthase in Soybean. Implications for Phytic Acid Biosynthesis. Plant Physiol. 2001;125(4):1941–8. doi: 10.1104/pp.125.4.1941 11299373

63. Donahue JL, Alford SR, Torabinejad J, Kerwin RE, Nourbakhsh A, Ray WK, et al. The Arabidopsis thaliana Myo-Inositol 1-Phosphate Synthase1 Gene Is Required for Myo-inositol Synthesis and Suppression of Cell Death. Plant Cell. 2010;22(3):888–903. doi: 10.1105/tpc.109.071779 20215587

64. Kusuda H, Koga W, Kusano M, Oikawa A, Saito K, Hirai MY, et al. Ectopic expression of myo-inositol 3-phosphate synthase induces a wide range of metabolic changes and confers salt tolerance in rice. Plant Sci. 2015;232:49–56. doi: 10.1016/j.plantsci.2014.12.009 25617323

65. Covarrubias L, Hernández-García D, Schnabel D, Salas-Vidal E, Castro-Obregón S. Function of reactive oxygen species during animal development: Passive or active? Dev Biol. 2008;320(1):1–11. doi: 10.1016/j.ydbio.2008.04.041 18555213

66. Jiménez-Quesada MJ, Traverso JÁ, Alché J de D. NADPH Oxidase-Dependent Superoxide Production in Plant Reproductive Tissues. Front Plant Sci. 2016;7(March):1–13.

67. Martin MV, Fiol DF, Sundaresan V, Zabaleta EJ, Pagnussat GC. oiwa, a Female Gametophytic Mutant Impaired in a Mitochondrial Manganese-Superoxide Dismutase, Reveals Crucial Roles for Reactive Oxygen Species during Embryo Sac Development and Fertilization in Arabidopsis. Plant Cell. 2013;25(5):1573–91. doi: 10.1105/tpc.113.109306 23653473

68. Ritter A, Goulitquer S, Salaün J-P, Tonon T, Correa JA, Potin P. Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol. 2008 Dec;180(4):809–21. doi: 10.1111/j.1469-8137.2008.02626.x 18823315

69. Di Dato V, Orefice I, Amato A, Fontanarosa C, Amoresano A, Cutignano A, et al. Animal-like prostaglandins in marine microalgae. ISME J. 2017 Jul 28;11(7):1722–6. doi: 10.1038/ismej.2017.27 28350392

70. Herpin A, Schartl M. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep. 2015 Oct 1;16(10):1260–74. doi: 10.15252/embr.201540667 26358957

71. Li W, Sullivan TD, Walton E, Averette AF, Sakthikumar S, Cuomo CA, et al. Identification of the Mating-Type (MAT) Locus That Controls Sexual Reproduction of Blastomyces dermatitidis. Eukaryot Cell. 2013 Jan;12(1):109–17. doi: 10.1128/EC.00249-12 23143684

72. Unk I, Hajdú I, Fátyol K, Szakál B, Blastyák A, Bermudez V, et al. Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc Natl Acad Sci. 2006;103(48):18107–12. doi: 10.1073/pnas.0608595103 17108083

73. Sun J, Yomogida K, Sakao S, Yamamoto H, Yoshida K, Watanabe K, et al. Rad18 is required for long-term maintenance of spermatogenesis in mouse testes. Mech Dev. 2009 Mar 1;126(3–4):173–83. doi: 10.1016/j.mod.2008.11.004 19068231

74. Richburg JH, Myers JL, Bratton SB. The role of E3 ligases in the ubiquitin-dependent regulation of spermatogenesis. Semin Cell Dev Biol. 2014 Jun 1;30:27–35. doi: 10.1016/j.semcdb.2014.03.001 24632385

75. Smith EA, Krumpelbeck EF, Jegga AG, Prell M, Matrka MM, Kappes F, et al. The nuclear DEK interactome supports multi-functionality. Proteins Struct Funct Bioinforma. 2018 Jan;86(1):88–97.

76. Maier I. New aspects of pheromone-triggered spermatozoid release in Laminaria digitata (Phaeophyta). Protoplasma. 1982;113(2):137–43.

77. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol. 2002;3(11):813–25. doi: 10.1038/nrm952 12415299

78. Fu G, Nagasato C, Oka S, Cock JM, Motomura T. Proteomics Analysis of Heterogeneous Flagella in Brown Algae (Stramenopiles). Protist. 2014;165(5):662–75. doi: 10.1016/j.protis.2014.07.007 25150613

79. Motomura T, Sakai Y. The occurrence of flagellated eggs in Laminaria angustata (Phaeophyta, Laminariales). J Phycol. 1988;24:282–5.

80. Klochkova TA, Motomura T, Nagasato C, Klimova A V., Kim GH. The role of egg flagella in the settlement and development of zygotes in two Saccharina species. Phycologia. 2019 Mar 4;58(2):145–53.

Sex-dependent and -independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima

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