3 Desiccation tolerance GRN in seeds and resurrection plants
Desiccation tolerance (DT), the ability to survive the loss of almost all cellular water without irreversible damage, appeared in the plant lineage during terrestrialization of their ancestor streptophyte algae (Figure 1) (Alpert, 2000; Leprince & Buitink, 2010; Oliver et al., 2000; Terlova, Holzinger, & Lewis, 2021; Wodniok et al., 2011). DT refers to survival after extreme dehydration (below 0.3 g H2O/g dry weight) where the cellular metabolic activity nearly stops, entering into a state of ‘anhydrobiosis’ (Hoekstra, Golovina, & Buitink, 2001).
At least six independent major clades of green algae were able to colonize dry environments and to display this remarkable ability to withstand extreme dehydration (Lewis & McCourt, 2004; Terlova et al., 2021). The initial appearance of DT features in the ancestor green algae was a crucial step for plant radiation on land (Oliver et al., 2000; Rensing et al., 2008; Wodniok et al., 2011). Vegetative DT is nowadays documented in about 68 bryophytes, 10 ferns and 10 angiosperms families (Artur, Costa, et al., 2019; Marks, Farrant, Nicholas McLetchie, & VanBuren, 2021; Oliver et al., 2020; Oliver et al., 2000). DT has been retained in reproductive structures (such as spores, pollen and seeds) of most land plant lineages, suggesting that virtually all plants display the genetic potential to become DT but are limited by morpho-physiological constraints (Alpert, 2000; Farrant & Moore, 2011; Marks, Farrant, et al., 2021; Oliver et al., 2000). It has been proposed that vegetative DT in Angiosperm resurrection plants re-evolved by re-directing common regulatory pathways from their reproductive structures (Costa et al., 2017; Farrant & Moore, 2011; Oliver et al., 2000). In fact, common morpho-physiological and biochemical signatures of DT have been found among evolutionarily distant resurrection plants, and between desiccation tolerant vegetative and reproductive structures. One example is the ability that certain groups of resurrection plants have to display leaf curling, rolling or folding, which provide protection against photo-damage during dehydration (‘homoichlorophylly’), while other groups undergo chlorophyll breakdown, chloroplast disassembly and synthesis of anthocyanin (‘poikilochlorophylly’), a common mechanism involved in seed acquisition of DT (Alpert, 2000; Artur, Zhao, et al., 2019; Charuvi et al., 2019; Dekkers et al., 2015; Radermacher, du Toit, & Farrant, 2019).
Recent developments in sequencing technologies are now also facilitating the assessment of genomic and regulatory adaptations underlying the origin and convergent 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). Comparison between desiccation tolerant and desiccation sensitive genomes and transcriptomes are revealing loss and repurposing of genes associated with the aquatic lifestyle of the ancestor green algae, and the expansion of gene families and refinement of gene expression necessary for survival on dry environments (Khraiwesh et al., 2015; Marks, Smith, VanBuren, & McLetchie, 2021; Peredo & Cardon, 2020; 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 in resurrection plants (Costa et al., 2017; Khraiwesh et al., 2015; Rensing et al., 2008; VanBuren et al., 2019; Xu et al., 2018). LEA genes are expressed during orthodox seed maturation, and their corresponding proteins accumulate when the seeds start to dry (Dure III, Galau, & Greenway, 1980; Dure et al., 1989; Galau, Hughes, & Dure, 1986; Verdier et al., 2013). These proteins are intrinsically disordered and can undergo disorder to-order transitions, what contribute to stabilization of membranes, organelles and the cytoplasm (Artur, Rienstra, et al., 2019; Buitink & Leprince, 2004; Crowe, Hoekstra, & Crowe, 1992; Wise & Tunnacliffe, 2004). A few LEA families were found to be commonly expanded in resurrection plant genomes, what indicates that specific LEAs contributed to the convergent evolution of DT in these species (Artur, Zhao, et al., 2019; Costa et al., 2017; VanBuren et al., 2017). Similarly, ELIPs, known to protect the cells against photooxidative damage under high light intensities (Hutin et al., 2003), have undergone a massive proliferation as tandem duplications in the genome of resurrection plants (VanBuren et al., 2019). Altogether, these studies are shedding light on common patterns of gene family expansion associated with convergent evolution of DT in resurrection plants.
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 brings 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). With more seed and resurrection plant genomes and transcriptomes becoming available, more information will be provided about the identity of the genes and pathways that underlie the convergent evolution of DT in different plant species and organs.