3 Desiccation tolerance in seeds and resurrection plants
As some plant lineages colonized drier lands, they developed desiccation
tolerance (DT), which is the ability to survive the loss of almost all
their cellular water without irreversible damage that would cause death
(Alpert, 2000; Leprince & Buitink, 2010; Oliver et al., 2000). DT
differs from drought tolerance as, based on critical water levels,
drought tolerance refers to survival after moderate dehydration
(approximately 0.3 g H2O/g dry weight) while DT
generally refers to survival after further dehydration (below 0.3 g
H2O/g dry weight) (Hoekstra, Golovina, & Buitink,
2001). Desiccation tolerant organisms are able to survive almost total
dehydration and enter into an ‘anhydrobiotic’ state of low metabolic
activity (Hoekstra et al., 2001). To enter into the anhydrobiotic state
a coordinated series of molecular events associated with prevention of
cellular damage takes place (Hoekstra et al., 2001; Oliver et al.,
2000).
It is believed that the initial appearance of DT features in vegetative
tissues of primitive plants was a crucial step for their colonization
and diversification on land (Oliver et al., 2000). As plants became more
complex organisms and started to colonize harsher environments, DT was
lost from vegetative tissues and became confined to reproductive
structures, such as pollen and (orthodox) seeds (Alpert, 2000; Farrant
& Moore, 2011; Oliver et al., 2000). A group of about 300 species
dispersed across 13 lineages of the plant phylogeny are known to display
common physiological, biochemical and molecular signatures of DT in
their vegetative structures, and are called ‘resurrection plants’
(Artur, Costa, et al., 2019; Oliver et al., 2020; Oliver et al., 2000).
Resurrection plants present two major strategies to tolerate
desiccation: ‘homoichlorophyllous’ resurrection plants display leaf
curling, rolling or folding, what provide protection against
photo-damage, while ‘poikilochlorophyllous’ resurrection plants undergo
chlorophyll breakdown, chloroplast disassembly and synthesis of
anthocyanin (Alpert, 2000; Artur, Zhao, et al., 2019; Charuvi et al.,
2019; Radermacher, du Toit, & Farrant, 2019). The recurring appearance
of these DT strategies across plant phylogeny gives a strong support for
the hypothesis of convergent evolution of DT, however, the features
underlying this phenomena were until recently unknown.
Recent developments in whole genome sequencing have facilitated the
assessment of the history of genes and regulatory pathways underlying
the 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). Comparative genomic studies
are now enabling the discovery of features underlying the recurrent
evolution of DT in plants (Artur, Zhao, et al., 2019; Costa et al.,
2017; Pardo et al., 2020; VanBuren et al., 2019). Comparison between
desiccation tolerant and desiccation sensitive genomes have revealed
loss of genes associated with the aquatic lifestyle of the ancestor
green algae, and the expansion of gene families and high expression of
genes necessary for light and dehydration protection (Khraiwesh et al.,
2015; 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 (Costa et al., 2017; Khraiwesh et al., 2015; Rensing et al.,
2008; VanBuren et al., 2019; Xu et al., 2018). LEA proteins were
discovered in cotton seeds as accumulating at the later stages of embryo
development during the maturation drying phase (Dure III, Galau, &
Greenway, 1980; Dure et al., 1989; Galau, Hughes, & Dure, 1986). These
proteins together with sugars, form intra-cellular glasses that
contribute with stabilization of membranes, organelles and the cytoplasm
(Artur, Rienstra, et al., 2019; Buitink & Leprince, 2004; Crowe,
Hoekstra, & Crowe, 1992; Wise & Tunnacliffe, 2004). LEAs belong to a
large protein family divided into eight groups (Artur, Zhao, et al.,
2019; Hundertmark & Hincha, 2008). The evolutionary analysis of the LEA
families has revealed expansion of specific subgroups in resurrection
plant genomes, suggesting that LEAs may have contributed with the
establishment of DT in these species (Artur, Zhao, et al., 2019; Costa
et al., 2017; VanBuren et al., 2017). ELIPs are known to protect the
cells against photooxidative damage under high light intensities (Hutin
et al., 2003). The analysis of the genomes of resurrection plants from
distant phylogenetic clades revealed a massive proliferation of ELIPs as
tandem duplications, supporting the hypothesis of convergent evolution
of DT in resurrection plants (VanBuren et al., 2019). ELIPs expansion
may have been especially important for homoiochlorophyllous species,
contributing to their ability to protect chloroplast structure and
chlorophyll during desiccation (VanBuren et al., 2019).
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 opens up 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).
Altogether these studies show the fundamental role of comparative
genomics and transcriptomics for the understanding of the evolution of
DT in plants. With more genomes and transcriptomes becoming available,
more information will be given for the co-option hypothesis of DT
between seeds and resurrection plants, contributing to the understanding
of how the underlying gene regulatory networks have convergently
evolved. These data will also provide knowledge about key TFs working
upstream of gene regulatory networks controlling DT pathways, which are
of potential interest for engeneering more drought tolerant crops.