1 Introduction
The transition of an ancestor aquatic green algae to a terrestrial
environment, termed terrestrialization, was a major event in the
evolution and diversification of the land plant flora. About 500Ma after
the first plant ancestor colonized the land, a multitude of adaptations
were developed allowing plants to cope with several problems such as
water scarcity (Becker & Marin, 2009; Delaux, Nanda, Mathé,
Sejalon-Delmas, & Dunand, 2012; Kenrick & Crane, 1997; Wodniok et al.,
2011). Some of the major adaptations to terrestrial lifestyle include
modification of the life cycle, divergence of the plant body into roots
and shoots, the appearance of complex phenolic compounds (e.g. lignin
and flavonoids), vascularization, and the development of specialized
cells (such as stomata) (Delaux et al., 2012). As they colonized land,
exposure to high radiations and drought became a recurring problem
encountered by multiple plant lineages, and common adaptations emerged
in diverging plant clades.
For example, photosynthesis under high light and low water availability
conditions became possible thanks to the recurring evolution of carbon
concentrating mechanisms (CCMs) across plant lineages. CCMs involve
either temporal or spatial separation of the initial carbon fixing from
the photosynthetic carbon fixing via anatomical adaptations (Edwards &
Ogburn, 2012). Studies have shown that all of the enzymes necessary for
the temporally separated CAM (Crassulacean Acid Metabolism) and the
spatially separated C4 metabolic pathways are present in
all plants and function in other processes (Burgess et al., 2016;
Christin et al., 2013; Dunning et al., 2019; Heyduk, Ray, et al., 2019;
Ming et al., 2015; Rondeau, Rouch, & Besnard, 2005; Yang et al., 2017).
The co-option of these enzymes for the appearance of the CCMs in
angiosperms was based on regulatory neofunctionalization of preexisting
genes, including those involved in C3 photosynthesis,
and rewiring of ancestral gene expression patterns (Figure 1) (Ming et
al., 2015; Yang et al., 2017).
Another clear example of convergent evolution of adaptations to dry
environments is desiccation tolerance (DT), which is the ability to
survive extreme drying and remain alive in the dry state (Alpert, 2000;
Leprince & Buitink, 2010; Oliver, Tuba, & Mishler, 2000). It has been
long hypothesized that DT mechanisms present in the vegetative body of
primitive bryophytes became confined in small reproductive structures
(such as spores, pollen and seeds) during the evolution of tracheophytes
(Figure 1) (Alpert, 2000; Oliver et al., 2000). Some plants were able to
colonize extremely dry environments by redirecting seed DT mechanimsms
into their vegetative body parts, the so-called resurrection plants
(Artur, Costa, Farrant, & Hilhorst, 2019; Farrant & Moore, 2011). This
co-option hypothesis has been recently assessed at the genomic level
thanks to the availability of whole genome sequences of resurrection
plants (Costa et al., 2017; Giarola, Hou, & Bartels, 2017; VanBuren et
al., 2018; VanBuren, Pardo, Man Wai, Evans, & Bartels, 2019; VanBuren
et al., 2017). Comparative genomics has recently revealed gene family
expansion and network rewiring underlying the convergent evolution of DT
(Artur, Zhao, Ligterink, Schranz, & Hilhorst, 2019; Oliver et al.,
2020; VanBuren et al., 2019).
Our final example is how hydrophobic extracellular biopolymers (such as
lignin, cutin and suberin) contribute to cell permeability and water
transport control, and are utilized also for critical drought tolerance
adaptations that have convergently evolved in plants. For example, it
was found that the ancestral green algae and red-algae were able to
produce “lignin-like” compounds (Delwiche, Graham, & Thomson, 1989;
Labeeuw, Martone, Boucher, & Case, 2015; Martone et al., 2009) and that
lycophytes and spermatophytes independently developed the ability to
produce monomers for lignin (Renault et al., 2017; Weng et al., 2010;
Weng, Li, Stout, & Chapple, 2008). Cutin and suberin seem to have also
independently evolved in different plant clades, as homologues of genes
encoding enzymes necessary for the biosynthesis of their precursors were
absent in ancestral non-angiosperm species (Cannell et al., 2020;
Philippe et al., 2020; Pollard, Beisson, Li, & Ohlrogge, 2008).
Furthermore, these biopolymers can be utilized in different cell types.
In some plant lineages suberin can play a role as a barrier for water
movement in the root exodermis in response to drought (Ejiri & Shiono,
2019; Enstone, Peterson, & Ma, 2002; Kreszies et al., 2020; Líška,
Martinka, Kohanová, & Lux, 2016; Reinhardt & Rost, 1995; Taleisnik,
Peyrano, Cordoba, & Arias, 1999). The exodermis possibly first appeared
in early land plants (lycophytes), and may have convergently evolved in
flowering plant lineages (Angiosperms) (Figure 1) (Perumalla, Peterson,
& Enstone, 1990).
The evolutionary hypothesis underlying the evolution of exodermis and
its role on drought adaptation, as well as DT and CCMs are largely
benefiting from recent advances in whole genome sequencing technologies
and comparative functional genomics. In this review, we provide an
overview of the current knowledge about how convergent evolution
contributed to the appearance of these adaptations to dry environments.