3 Desiccation tolerance in seeds and resurrection plants
As some plant lineages colonized drier lands, they developed desiccation tolerance (DT), which is the ability to survive the loss of almost all their cellular water without irreversible damage that would cause death (Alpert, 2000; Leprince & Buitink, 2010; Oliver et al., 2000). DT differs from drought tolerance as, based on critical water levels, drought tolerance refers to survival after moderate dehydration (approximately 0.3 g H2O/g dry weight) while DT generally refers to survival after further dehydration (below 0.3 g H2O/g dry weight) (Hoekstra, Golovina, & Buitink, 2001). Desiccation tolerant organisms are able to survive almost total dehydration and enter into an ‘anhydrobiotic’ state of low metabolic activity (Hoekstra et al., 2001). To enter into the anhydrobiotic state a coordinated series of molecular events associated with prevention of cellular damage takes place (Hoekstra et al., 2001; Oliver et al., 2000).
It is believed that the initial appearance of DT features in vegetative tissues of primitive plants was a crucial step for their colonization and diversification on land (Oliver et al., 2000). As plants became more complex organisms and started to colonize harsher environments, DT was lost from vegetative tissues and became confined to reproductive structures, such as pollen and (orthodox) seeds (Alpert, 2000; Farrant & Moore, 2011; Oliver et al., 2000). A group of about 300 species dispersed across 13 lineages of the plant phylogeny are known to display common physiological, biochemical and molecular signatures of DT in their vegetative structures, and are called ‘resurrection plants’ (Artur, Costa, et al., 2019; Oliver et al., 2020; Oliver et al., 2000). Resurrection plants present two major strategies to tolerate desiccation: ‘homoichlorophyllous’ resurrection plants display leaf curling, rolling or folding, what provide protection against photo-damage, while ‘poikilochlorophyllous’ resurrection plants undergo chlorophyll breakdown, chloroplast disassembly and synthesis of anthocyanin (Alpert, 2000; Artur, Zhao, et al., 2019; Charuvi et al., 2019; Radermacher, du Toit, & Farrant, 2019). The recurring appearance of these DT strategies across plant phylogeny gives a strong support for the hypothesis of convergent evolution of DT, however, the features underlying this phenomena were until recently unknown.
Recent developments in whole genome sequencing have facilitated the assessment of the history of genes and regulatory pathways underlying the 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). Comparative genomic studies are now enabling the discovery of features underlying the recurrent evolution of DT in plants (Artur, Zhao, et al., 2019; Costa et al., 2017; Pardo et al., 2020; VanBuren et al., 2019). Comparison between desiccation tolerant and desiccation sensitive genomes have revealed loss of genes associated with the aquatic lifestyle of the ancestor green algae, and the expansion of gene families and high expression of genes necessary for light and dehydration protection (Khraiwesh et al., 2015; 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 (Costa et al., 2017; Khraiwesh et al., 2015; Rensing et al., 2008; VanBuren et al., 2019; Xu et al., 2018). LEA proteins were discovered in cotton seeds as accumulating at the later stages of embryo development during the maturation drying phase (Dure III, Galau, & Greenway, 1980; Dure et al., 1989; Galau, Hughes, & Dure, 1986). These proteins together with sugars, form intra-cellular glasses that contribute with stabilization of membranes, organelles and the cytoplasm (Artur, Rienstra, et al., 2019; Buitink & Leprince, 2004; Crowe, Hoekstra, & Crowe, 1992; Wise & Tunnacliffe, 2004). LEAs belong to a large protein family divided into eight groups (Artur, Zhao, et al., 2019; Hundertmark & Hincha, 2008). The evolutionary analysis of the LEA families has revealed expansion of specific subgroups in resurrection plant genomes, suggesting that LEAs may have contributed with the establishment of DT in these species (Artur, Zhao, et al., 2019; Costa et al., 2017; VanBuren et al., 2017). ELIPs are known to protect the cells against photooxidative damage under high light intensities (Hutin et al., 2003). The analysis of the genomes of resurrection plants from distant phylogenetic clades revealed a massive proliferation of ELIPs as tandem duplications, supporting the hypothesis of convergent evolution of DT in resurrection plants (VanBuren et al., 2019). ELIPs expansion may have been especially important for homoiochlorophyllous species, contributing to their ability to protect chloroplast structure and chlorophyll during desiccation (VanBuren et al., 2019).
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 opens up 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).
Altogether these studies show the fundamental role of comparative genomics and transcriptomics for the understanding of the evolution of DT in plants. With more genomes and transcriptomes becoming available, more information will be given for the co-option hypothesis of DT between seeds and resurrection plants, contributing to the understanding of how the underlying gene regulatory networks have convergently evolved. These data will also provide knowledge about key TFs working upstream of gene regulatory networks controlling DT pathways, which are of potential interest for engeneering more drought tolerant crops.