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New features of desiccation tolerance in the lichen photobiont Trebouxia gelatinosa are revealed by a transcriptomic approach

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Abstract

Trebouxia is the most common lichen-forming genus of aero-terrestrial green algae and all its species are desiccation tolerant (DT). The molecular bases of this remarkable adaptation are, however, still largely unknown. We applied a transcriptomic approach to a common member of the genus, T. gelatinosa, to investigate the alteration of gene expression occurring after dehydration and subsequent rehydration in comparison to cells kept constantly hydrated. We sequenced, de novo assembled and annotated the transcriptome of axenically cultured T. gelatinosa by using Illumina sequencing technology. We tracked the expression profiles of over 13,000 protein-coding transcripts. During the dehydration/rehydration cycle c. 92 % of the total protein-coding transcripts displayed a stable expression, suggesting that the desiccation tolerance of T. gelatinosa mostly relies on constitutive mechanisms. Dehydration and rehydration affected mainly the gene expression for components of the photosynthetic apparatus, the ROS-scavenging system, Heat Shock Proteins, aquaporins, expansins, and desiccation related proteins (DRPs), which are highly diversified in T. gelatinosa, whereas Late Embryogenesis Abundant Proteins were not affected. Only some of these phenomena were previously observed in other DT green algae, bryophytes and resurrection plants, other traits being distinctive of T. gelatinosa, and perhaps related to its symbiotic lifestyle. Finally, the phylogenetic inference extended to DRPs of other chlorophytes, embryophytes and bacteria clearly pointed out that DRPs of chlorophytes are not orthologous to those of embryophytes: some of them were likely acquired through horizontal gene transfer from extremophile bacteria which live in symbiosis within the lichen thallus.

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Acknowledgments

The study was funded by the Italian Ministry of Education, University, and Research under the PRIN 2010-11 project “TreeCity—Planning the green city in the global change era: urban tree functions and suitability for predicted future climates”, and by University of Trieste (“Finanziamento di Ateneo per la Ricerca Scientifica 2011”), local resp. M. T. The activity of F. C. C. was partially funded by a DIANET post-doc outgoing fellowship grant. The activity of E. B. was funded by the Italian Government Commission with “Fondo Trieste”. We thank Dr. Gabriele Leoni (Trieste) for technical help.

Author contributions

FCC wrote the manuscript, took part in the experimental design development and in the growth of Trebouxia cultures; MG wrote the manuscript and performed the bioinformatic analyses; AM took part in the experimental design, performed the isolation of Trebouxia, the RNA extraction and contributed in the bioinformatic analyses; EB performed the qRT-PCR analysis and produced the manuscript figures and tables; GDM performed the de novo assembly and annotation of the transcriptome; CM contributed in the extraction and purification of the RNAs; LM contributed in the isolation and identification of the Trebouxia photobiont and co-edited the manuscript; AP took part in the experimental design development and managed RNA sequencing and bioinformatic analyses; MT is the project supervisor, he took part in the experimental design development and co-edited the manuscript. All the authors critically contributed to the discussion of the manuscript and approved the final version

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    1. Dipartimento di Scienze della Vita, Università degli Studi di Trieste, via L. Giorgieri, 10, 34127, Trieste, Italy

      Fabio Candotto Carniel, Marco Gerdol, Alice Montagner, Elisa Banchi, Gianluca De Moro, Chiara Manfrin, Lucia Muggia, Alberto Pallavicini & Mauro Tretiach

    2. Institute of Botany, University of Innsbruck, Sternwartestraße, 15, 6020, Innsbruck, Austria

      Fabio Candotto Carniel

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    1. Fabio Candotto Carniel
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    Correspondence to Marco Gerdol.

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    Fabio Candotto Carniel and Marco Gerdol have contributed equally to this work.

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    Carniel, F.C., Gerdol, M., Montagner, A. et al. New features of desiccation tolerance in the lichen photobiont Trebouxia gelatinosa are revealed by a transcriptomic approach. Plant Mol Biol 91, 319–339 (2016). https://doi.org/10.1007/s11103-016-0468-5

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