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An Intracellular Transcriptomic Atlas of the Giant Coenocyte


Plants include both the green algae and land plants. Multiple times, root, stem, and leaf-like structures arose independently in plant lineages. In some instances, such as the siphonous algae, these structures arose in the absence of multicellularity. It has been argued by some that the morphology of multicellular land plant organs similarly arises independently of cell division patterns. Here, we explore the partitioning of gene transcripts within what is debatably the largest single-celled organism in the world, the siphonous alga Caulerpa taxifolia. We find that within this giant cell specific transcripts localize within pseudo-organs (morphological structures that are not comprised of cells or tissue). The overall pattern of transcript accumulation follows an apical-basal pattern within the cell. Moreover, transcripts related to different cellular processes, such as transcription and translation, localize to specific regions. Analyzing the signatures of transcript accumulation in land plant organs and the pseudo-organs of Caulerpa, we find that groups of transcripts accumulate together in morphological structures across evolution at rates higher than expected by chance. Together, our results demonstrate a relationship between transcript partitioning and organism morphology, independent from multicellularity, throughout diverse plant lineages.


Vyšlo v časopise: An Intracellular Transcriptomic Atlas of the Giant Coenocyte. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004900
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004900

Souhrn

Plants include both the green algae and land plants. Multiple times, root, stem, and leaf-like structures arose independently in plant lineages. In some instances, such as the siphonous algae, these structures arose in the absence of multicellularity. It has been argued by some that the morphology of multicellular land plant organs similarly arises independently of cell division patterns. Here, we explore the partitioning of gene transcripts within what is debatably the largest single-celled organism in the world, the siphonous alga Caulerpa taxifolia. We find that within this giant cell specific transcripts localize within pseudo-organs (morphological structures that are not comprised of cells or tissue). The overall pattern of transcript accumulation follows an apical-basal pattern within the cell. Moreover, transcripts related to different cellular processes, such as transcription and translation, localize to specific regions. Analyzing the signatures of transcript accumulation in land plant organs and the pseudo-organs of Caulerpa, we find that groups of transcripts accumulate together in morphological structures across evolution at rates higher than expected by chance. Together, our results demonstrate a relationship between transcript partitioning and organism morphology, independent from multicellularity, throughout diverse plant lineages.


Zdroje

1. HämmerlingJ (1953) Nucleo-cytoplasmic relationship in the development of Acetabularia. J Intern Rev Cytol 2: 475–498.

2. MandoliDF (1992) Vegetative growth of Acetabularia acetabulum (Chlorophyta): Structural evidence for juvenile and adult phases in development. Journal of Phycology 5: 669–677.

3. MandoliDF (1998) Elaboration of body plan and phase change during development of Acetabularia: How is the complex architecture of a giant unicell built? Annual review of plant biology 49: 173–198.

4. DawesCJ, RhamstineE (1967) An ultra-structural study of the giant algal coenocyte, Caulerpa prolifera. J Phycol 3: 177–126.

5. DawesCJ, BarilottiDC (1969) Cytoplasmic organization and rhythmic streaming in growing blades of Caulerpa prolifera. Amer J Bot 56: 8–15.

6. JacobsWP, OlsonJ (1980) Developmental changes in the algal coenocyte Caulerpa prolifera (Siphonales) after inversion with respect to gravity. Amer J Bot 67: 141–146.

7. MenzelD, GrantBR (1981) Fine structure study on the development of trabeculae in the siphonous green alga Caulerpa simpliciuscula C. Ag. Protoplasma 107: 47–61.

8. MatilskyMB, JacobsWP (1983) Regeneration in the coenocytic marine alga, Caulerpa, with respect to gravity. American Journal of Botany 70: 635–638.

9. ChisholmJR, DaugaC, AgeronE, GrimontPA, JaubertJM (1996) ‘Roots’ in mixotrophic algae. Nature 381: 382.

10. Schwann T, Schleiden MJ (1847) Microscopical researches into the accordance in the structure and growth of animals and plants. London: Printed for the Sydenham Society.

11. Kaplan DR, Hagemann W (1991) The relationship of cell and organism in vascular plants. Bioscience 693–703

12. KapraunDR (2005) Nuclear DNA content estimates in multicellular green, red, and brown algae: phylogenetic considerations. Annals of Botany 95: 7–44.

13. Varela-ÁlvarezE, Gómez GarretaA, Rull LluchJ, Salvador SolerN, SerraoEA, et al. (2012) Mediterranean species of Caulerpa are polyploidy with smaller genomes in the invasive ones. PLOS ONE 7: e47728.

14. JanseJM (1910) Über Organveränderung bei Caulerpa prolifera. Jahrb. Wiss Bot 48: 73–110.

15. KumarR, IchihashiY, KimuraS, ChitwoodDH, HeadlandLR, et al. (2012) A High-Throughput Method for Illumina RNA-Seq Library Preparation. Front Plant Sci 3: 202.

16. KoenigD, Jiménez-GómezJM, KimuraS, FulopD, ChitwoodDH, et al. (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci USA 110: E2655–62.

17. ChitwoodDH, MaloofJN, SinhaNR (2013) Dynamic transcriptomic profiles between tomato and a wild relative reflect distinct revelopmental architectures. Plant Physiol 162: 537–52.

18. SessionsA, YanofskyMF, WeigelD (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289: 779–82.

19. NakajimaK, SenaG, NawyT, BenfeyPN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413: 307–11.

20. ChitwoodDH, NogueiraFT, HowellMD, MontgomeryTA, CarringtonJC, et al. (2009) Pattern formation via small RNA mobility. Genes Dev 23: 549–54.

21. CarlsbeckerA, LeeJY, RobertsCJ, DettmerJ, LehesrantaS, et al. (2010) Cell signaling by microRNA 165/6 directs gene dose-dependent root cell fate. Nature 465: 316–21.

22. MenzelD, Elsner-MenzelC (1989) Actin-based chloroplast rearrangements in the cortex of the giant coenocytic green alga Caulerpa. Protoplasma 150: 1–8.

23. RanjanA, IchihashiY, FarhiM, ZumsteinK, TownsleyB, et al. (2014) De novo assembly and characterization of the transcriptome of the parasitic weed Cuscuta pentagona identifies genes associated with plant parasitism. Plant Physiol 166: 1186–99.

24. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644–652.

25. GoffSA, VaughnM, McKayS, LyonsE, StapletonAE, et al. (2011) The iPlant Collaborative: Cyberinfrastructure for Plant Biology. Front Plant Sci 2: 34.

26. HuangY, NiuB, GaoY, FuL, LiW (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680–682.

27. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

28. GotzS, Garcia-GomezJM, TerolJ, WilliamsTD, NagarajSH, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420–3435.

29. LiuS, LiW, WuY, ChenC, LeiJ (2013) De novo transcriptome assembly in chili pepper (Capsicum frutescens) to identify genes involved in the biosynthesis of capsaicinoids. PLOS ONE 8: e48156.

30. NakasugiK, CrowhurstRN, BallyJ, WoodCC, HellensRP, et al. (2013) De novo transcriptome sequence assembly and analysis of RNA silencing genes of Nicotiana benthamiana. PLOS ONE 8: e59534.

31. LiB, DeweyCN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.

32. RobinsonMD, OshlackA (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.

33. HaasBJ, PapanicolaouA, YassourM, GrabherrM, BloodPD, et al. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8: 1494–1512.

34. Kohonen T (1997) Self-Organizing Maps. Springer, New York.

35. WehrensR, BuydensLMC (2007) Self- and super-organizing maps in R: the Kohonen package. J Stat Softw 21: 1–19.

36. R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.

37. Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth Edition. New York: Springer.

38. YoungMD, WakefieldMJ, SmythGK, OshlackA (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11: R14.

39. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York.

40. CocquytE, VerbruggenH, LeliaertF, De ClerckO (2010) Evolution and cytological diversification of the green seweeds (Ulvophyceae). Mol Biol Evol 27: 2052–61.

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Genetika Reprodukčná medicína

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PLOS Genetics


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