New features of desiccation tolerance in the lichen photobiont
Trebouxia gelatinosa are revealed by a transcriptomic approach
Fabio Candotto Carniel
Gianluca De Moro
Received: 17 September 2015 / Accepted: 4 March 2016 / Published online: 18 March 2016
Ó Springer Science+Business Media Dordrecht 2016
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 tran-
scriptome 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.
Keywords Aero-terrestrial microalgae Á Desiccation
related proteins Á Gene expression Á Illumina Á
Lichenization Á Trebouxiophyceae
Poikilohydric organisms are able to colonize very harsh
environments, such as hot and cold deserts, rock surfaces
or tree barks, thanks to their ability to survive extreme
desiccation states and to recover full metabolic activity
within minutes to hours upon rewetting (Lide
n et al. 2010).
This ability is commonly known as desiccation tolerance. It
is documented in cyanobacteria (Bu
del 2011), aeroterres-
trial micro-algae (Trainor and Gladych 1995; Holzinger
and Karsten 2013), intertidal algae (Bu
del 2011), bryo-
phytes (Richardson and Richardson 1981; Proctor 1990;
Proctor et al. 2007), lichens (Mazur 1968; Kranner et al.
2008), and a few vascular plants, the so-called resurrection
plants (Proctor and Tuba 2002). It also occurs among
heterotrophs, such as tardigrades (Wright 2001), nematodes
(Treonis and Wall 2005), and arthropods (Kikawada et al.
2005). This capability may be extended to the whole life
cycle of the organism, or it may involve just some stages,
as it happens in ﬂowering plants, whose pollen grains and
Fabio Candotto Carniel and Marco Gerdol have contributed equally to
Electronic supplementary material The online version of this
article (doi:10.1007/s11103-016-0468-5) contains supplementary
material, which is available to authorized users.
& Marco Gerdol
Dipartimento di Scienze della Vita, Universita
degli Studi di
Trieste, via L. Giorgieri, 10, 34127 Trieste, Italy
Institute of Botany, University of Innsbruck,
Sternwartestraße, 15, 6020 Innsbruck, Austria
Plant Mol Biol (2016) 91:319–339