3 Desiccation tolerance GRN in seeds and resurrection plants
Desiccation tolerance (DT), the ability to survive the loss of almost
all cellular water without irreversible damage, appeared in the plant
lineage during terrestrialization of their ancestor streptophyte algae
(Figure 1) (Alpert, 2000; Leprince & Buitink, 2010; Oliver et al.,
2000; Terlova, Holzinger, & Lewis, 2021; Wodniok et al., 2011). DT
refers to survival after extreme dehydration (below 0.3 g
H2O/g dry weight) where the cellular metabolic activity
nearly stops, entering into a state of ‘anhydrobiosis’ (Hoekstra,
Golovina, & Buitink, 2001).
At least six independent major clades of green algae were able to
colonize dry environments and to display this remarkable ability to
withstand extreme dehydration (Lewis & McCourt, 2004; Terlova et al.,
2021). The initial appearance of DT features in the ancestor green algae
was a crucial step for plant radiation on land (Oliver et al., 2000;
Rensing et al., 2008; Wodniok et al., 2011). Vegetative DT is nowadays
documented in about 68 bryophytes, 10 ferns and 10 angiosperms families
(Artur, Costa, et al., 2019; Marks, Farrant, Nicholas McLetchie, &
VanBuren, 2021; Oliver et al., 2020; Oliver et al., 2000). DT has been
retained in reproductive structures (such as spores, pollen and seeds)
of most land plant lineages, suggesting that virtually all plants
display the genetic potential to become DT but are limited by
morpho-physiological constraints (Alpert, 2000; Farrant & Moore, 2011;
Marks, Farrant, et al., 2021; Oliver et al., 2000). It has been proposed
that vegetative DT in Angiosperm resurrection plants re-evolved by
re-directing common regulatory pathways from their reproductive
structures (Costa et al., 2017; Farrant & Moore, 2011; Oliver et al.,
2000). In fact, common morpho-physiological and biochemical signatures
of DT have been found among evolutionarily distant resurrection plants,
and between desiccation tolerant vegetative and reproductive structures.
One example is the ability that certain groups of resurrection plants
have to display leaf curling, rolling or folding, which provide
protection against photo-damage during dehydration
(‘homoichlorophylly’), while other groups undergo chlorophyll breakdown,
chloroplast disassembly and synthesis of anthocyanin
(‘poikilochlorophylly’), a common mechanism involved in seed acquisition
of DT (Alpert, 2000; Artur, Zhao, et al., 2019; Charuvi et al., 2019;
Dekkers et al., 2015; Radermacher, du Toit, & Farrant, 2019).
Recent developments in sequencing technologies are now also facilitating
the assessment of genomic and regulatory adaptations underlying the
origin and convergent evolution of DT in plants. In the past five years,
at least eight whole genomes and several transcriptomes of desiccation
tolerant plant species from distinct phylogenetic groups became
available (Artur, Costa, et al., 2019; Oliver et al., 2020). Comparison
between desiccation tolerant and desiccation sensitive genomes and
transcriptomes are revealing loss and repurposing of genes associated
with the aquatic lifestyle of the ancestor green algae, and the
expansion of gene families and refinement of gene expression necessary
for survival on dry environments (Khraiwesh et al., 2015; Marks, Smith,
VanBuren, & McLetchie, 2021; Peredo & Cardon, 2020; Rensing et al.,
2008; VanBuren et al., 2019; Xu et al., 2018). The latter is clearly
exemplified by expansion of late embryogenesis abundant proteins (LEAs)
and early-light induced proteins (ELIPs) families in resurrection plants
(Costa et al., 2017; Khraiwesh et al., 2015; Rensing et al., 2008;
VanBuren et al., 2019; Xu et al., 2018). LEA genes are expressed during
orthodox seed maturation, and their corresponding proteins accumulate
when the seeds start to dry (Dure III, Galau, & Greenway, 1980; Dure et
al., 1989; Galau, Hughes, & Dure, 1986; Verdier et al., 2013). These
proteins are intrinsically disordered and can undergo disorder to-order
transitions, what contribute to stabilization of membranes, organelles
and the cytoplasm (Artur, Rienstra, et al., 2019; Buitink & Leprince,
2004; Crowe, Hoekstra, & Crowe, 1992; Wise & Tunnacliffe, 2004). A few
LEA families were found to be commonly expanded in resurrection plant
genomes, what indicates that specific LEAs contributed to the convergent
evolution of DT in these species (Artur, Zhao, et al., 2019; Costa et
al., 2017; VanBuren et al., 2017). Similarly, ELIPs, known to protect
the cells against photooxidative damage under high light intensities
(Hutin et al., 2003), have undergone a massive proliferation as tandem
duplications in the genome of resurrection plants (VanBuren et al.,
2019). Altogether, these studies are shedding light on common patterns
of gene family expansion associated with convergent evolution of DT in
resurrection plants.
Usually, angiosperm resurrection plants respond to vegetative
desiccation by inducing the expression of regulatory pathways typically
related to seed DT (Costa et al., 2017; Giarola et al., 2017; Pardo et
al., 2020; VanBuren et al., 2017). A recent study has shown, however,
that despite conserved seed regulatory networks being activated in
vegetative tissues of the poikilochlorophyllous resurrection plantXerophyta humilis , the master transcription factors (TFs)
upstream of these pathways in seeds are not activated in vegetative
tissues (Lyall et al., 2020). This finding brings novel hypotheses about
the evolution of DT. For example, it is likely that the activation of
components of seed DT in vegetative tissues involved the appearance of
alternative TFs that have evolved in a similar fashion in different
resurrection plant genomes. A comparative genome and transcriptome study
have recently shown that seed dehydration-related genes shared similar
expression patterns among desiccation tolerant and sensitive grass
species during drought, however, subsets of seed-specific genes were
identified as expressing only in desiccation tolerant grasses (Pardo et
al., 2020). With more seed and resurrection plant genomes and
transcriptomes becoming available, more information will be provided
about the identity of the genes and pathways that underlie the
convergent evolution of DT in different plant species and organs.