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:
- How do GRNs convergently evolve to adapt to dry environments?
- Are the same genes and GRNs co-opted or repurposed during independent
evolutions?
- What are the shared ancestral GRNs for these traits? What makes
ancestral GRNs predisposed for convergent co-option or repurposing?
- What are the different, not shared pathways taken during independent
evolutions?
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.