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 ancestor colonized the land, the appearance of a multitude of morpho-physiological adaptations allowed plants to cope with several problems related to terrestrial life, 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 at the cell, tissue and organ levels emerged in diverging plant clades. It was until recently unknown how these morpho-physiological adaptations evolved on a genetic level in phylogenetically distant plant species.
Recent advances on whole genome and transcriptome sequencing are now providing evidence that co-option of genes and gene regulatory networks (GRNs) underlies the appearance of cell, organ and tissue level adaptations to dry environments. For example, carbon concentrating mechanisms (CCMs) allow photosynthesis under high light and low water availability conditions and 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, Moreno-Villena, et al., 2019; Heyduk, Ray, et al., 2019; Rondeau, Rouch, & Besnard, 2005; Yang et al., 2017). The co-option of these enzymes for CCMs was based on regulatory co-option and neofunctionalization of pre-existing genes, including those involved in C3 photosynthesis, and rewiring of ancestral GRNs (Figure 1) (Ming et al., 2015; Yang et al., 2017).
Another clear example of plant adaptation to dry environments is desiccation tolerance (DT), 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 ancestral land plants became confined in small reproductive organs, such as seeds, during the evolution of tracheophytes (Figure 1) (Alpert, 2000; Oliver et al., 2000). These DT mechanisms of seeds were then co-opted in the vegetative body of angiosperm ‘resurrection plants’ to be able to survive in extremely dry environments (Artur, Costa, Farrant, & Hilhorst, 2019; Farrant & Moore, 2011). The co-option of DT genes and GRNs has been recently assessed in the genome and transcriptome 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 genomic studies are also revealing that similar gene families and GRNs have expanded and/or being rewired similarly in multiple resurrection plants (Artur, Zhao, Ligterink, Schranz, & Hilhorst, 2019; Oliver et al., 2020; VanBuren et al., 2019).
The production of hydrophobic extracellular biopolymers (such as lignin, cutin and suberin) is also an important adaptation to survive on dry land that appeared in specific cells, tissues and organs of diverging plant clades. Comparative genome studies have shown that the ancestral green algae and red-algae were already able to produce “lignin-like” compounds (Delwiche, Graham, & Thomson, 1989; Labeeuw, Martone, Boucher, & Case, 2015; Martone et al., 2009) but lycophytes and spermatophytes seem to have 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). The co-option of GRNs for the biosynthesis of these biopolymers in specific root cell types has likely contributed to plant plasticity on dry land. For example, suberin is known to dynamically form barrier for water movement in root endodermis, and it also contributes to plant acclimation to drought when deposited in the exodermis (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 evolution of exodermis remains poorly understood. A suberized exodermis possibly first appeared in early land plants (lycophytes). Its plasticity may have involved the co-option of regulatory genes from the endodermis, and may have convergently occurred in some flowering plant lineages (Angiosperms) submitted to constant environmental water fluctuations (Figure 1) (Perumalla, Peterson, & Enstone, 1990). Due to the coexistence of endodermis and exodermis in roots, separation of these cell types for gene expression analyses has been required to understand which genes and GRNs are active in each cell type, and to assess co-option and innovation in exodermis GRN evolution (Kajala et al., 2021; Shiono et al., 2014).
In addition to CCMs, DT and root impermeabilization, there are many other adaptations to dry environments that have evolved convergently; such as succulence (Griffiths & Males, 2017), leaf shape (Nicotra et al., 2011; Peguero-Pina et al., 2020) and shallow root system architecture (Griffiths & Males, 2017). However, in this review, we focus on the current knowledge about genes and GRNs recently found to be involved with the convergent evolution of CCMs, DT and root impermeabilization in different plant clades. Using these three examples, we provide insight in the current state of understanding of the following gaps in knowledge:
We will also address how functional genomics can help to generate and to test the novel hypotheses about the evolution and function of these genes.