Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae

Abstract

<jats:p>Among green plants, desiccation tolerance is common in seeds and spores but rare in leaves and other vegetative green tissues. Over the last two decades, genes have been identified whose expression is induced by desiccation in diverse, desiccation-tolerant (DT) taxa, including, e.g., late embryogenesis abundant proteins (LEA) and reactive oxygen species scavengers. This up-regulation is observed in DT resurrection plants, mosses, and green algae most closely related to these Embryophytes. Here we test whether this same suite of protective genes is up-regulated during desiccation in even more distantly related DT green algae, and, importantly, whether that up-regulation is unique to DT algae or also occurs in a desiccation-intolerant relative. We used three closely related aquatic and desert-derived green microalgae in the family Scenedesmaceae and capitalized on extraordinary desiccation tolerance in two of the species, contrasting with desiccation intolerance in the third. We found that during desiccation, all three species increased expression of common protective genes. The feature distinguishing gene expression in DT algae, however, was extensive down-regulation of gene expression associated with diverse metabolic processes during the desiccation time course, suggesting a switch from active growth to energy-saving metabolism. This widespread downshift did not occur in the desiccation-intolerant taxon. These results show that desiccation-induced up-regulation of expression of protective genes may be necessary but is not sufficient to confer desiccation tolerance. The data also suggest that desiccation tolerance may require induced protective mechanisms operating in concert with massive down-regulation of gene expression controlling numerous other aspects of metabolism.</jats:p>

Patterns of gene expression in pollen of cotton (Gossypium hirsutum) indicate down-regulation as a feature of thermotolerance

“…Moreover, a study on desiccation-tolerant and -intolerant algae revealed that all taxa upregulated critical protective genes, whereas the tolerant taxon down-regulated cellular metabolism during water stress to conserve energy (Peredo and Cardon, 2020). Those genes involved in slowing down metabolism at the AN and LE stages under heat are likely to confer thermotolerance; these candidates should be further investigated as the basis of thermotolerance traits in susceptible species and tissues.…”

“…However, the increased m-RNAs under stress and limited splicing machinery, lead to splicing errors in heat-responsive genes. On the other hand, recent studies have demonstrated that down-regulation of non-essential pathways is undertaken by tolerant species to overcome stress conditions (Peredo and Cardon, 2020;Voesenek and Bailey-Serres, 2013). The new perspective on tolerance of plants proposes that up-regulation of protective genes must be warranted but the metabolism of cells should undergo an extensive downregulation in response to abiotic stress, such as high temperature.…”

Analysis of Stop Codons within Prokaryotic Protein-Coding Genes Suggests Frequent Readthrough Events

“…Thus, it is likely that a decrease in expression due to presence of in-frame stop codons is beneficial for functioning of prokaryotic cells (at least, for short periods of time). Importance of the gene downregulation in response to various factors has been shown for various pro- and eukaryotic species [ 51 , 52 , 53 , 54 , 55 ].…”

Convergent evolution of gene regulatory networks underlying plant adaptations to dry environments

“…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).…”