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.