A comparative gene co-expression analysis using self-organizing maps on two congener filmy ferns identifies specific desiccation tolerance mechanisms associated to their microhabitat preference

Abstract

Background: Filmy-ferns (Hymenophyllaceae) are poikilohydric, homoiochlorophyllous desiccation-tolerant (DT) epiphytes. They can colonize lower and upper canopy environments of humid forest. Filmy-ferns desiccate rapidly (hours), contrasting with DT angiosperms (days/weeks). It has been proposed that desiccation tolerance in filmyferns would be associated mainly with constitutive features rather than induced responses during dehydration. However, we hypothesize that the inter-specific differences in vertical distribution would be associated with different dynamics of gene expression within the dehydration or rehydration phases. A comparative transcriptomic analysis with an artificial neural network was done on Hymenophyllum caudiculatum (restricted to lower canopy) and Hymenophyllum dentatum (reach upper canopy) during a desiccation/rehydration cycle. Results: Raw reads were assembled into 69,599 transcripts for H. dentatum and 34,726 transcripts for H. caudiculatum. Few transcripts showed significant changes in differential expression (DE). H. caudiculatum had ca. twice DE genes than H. dentatum and higher proportion of increased-and-decreased abundance of genes occurs during dehydration. In contrast, the abundance of genes in H. dentatum decreased significantly when transitioning from dehydration to rehydration. According to the artificial neural network results, H. caudiculatum enhanced osmotic responses and phenylpropanoid related pathways, whilst H. dentatum enhanced its defense system responses and protection against high light stress. Conclusions: Our findings provide a deeper understanding of the mechanisms underlying the desiccation tolerance responses of two filmy ferns and the relationship between the species-specific response and the microhabitats these ferns occupy in nature.

Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae)

“…Vegetative DT was a key innovation linked to the rise of early land plants, but is largely limited to non-vascular groups such as bryophytes and algae among extant plants. Filmy ferns have received considerable attention for their remarkable reversion to vegetative DT in the sporophyte phase (e.g., Cea et al 2014;Ostria-Gallardo et al 2020a;Proctor 2003;Shreve 1911). Yet, no previous study to our knowledge has evaluated parallel physiology of sporophytes and gametophytes of filmy ferns in relation to DT.…”

“…This was further supported by evidence that induced biomechanical mechanisms likely do not play a role in DT of filmy ferns (Fallard et al 2018; but see Mkhize et al 2020). Recently, transcriptomics has been applied to elucidate the genes involved at each step of the desiccation-recovery cycle of filmy ferns (Ostria-Gallardo et al 2020a;b).…”

“…Future studies of DT in filmy ferns should include juvenile stages of the sporophyte, which are expected to experience similar microhabitats as gametophytes, to better determine the role of microhabitat vs. life stage (and plant size) on DT. The recent application of transcriptomics to filmy fern ecophysiology has begun to reveal the genetic mechanisms underlying DT in these plants (Ostria-Gallardo et al 2020a;b). Future studies that apply such methods to gametophytes as well as sporophytes across a variety of growth habits are anticipated to provide even greater insight into the ecology and evolution of filmy ferns as well as the transition from desiccation tolerance to avoidance in vascular plants.…”

Decoding Gene Networks Modules That Explain the Recovery of Hymenoglossum cruentum Cav. After Extreme Desiccation

“…This becomes relevant considering that RNA molecules (particularly mRNA) are the way in which cells carry out the instructions encoded in the DNA. To our knowledge, there is very limited information about the transcriptional dynamic associated to dehydration-rehydration in Hymenophyllaceae species (Ostria-Gallardo et al, 2020). Thus, FIGURE 3 | Comparison of the change in expression during the desiccation-rehydration process of candidate genes that would be pivotal in the desiccation tolerance response of H. cruentum by quantification of real-time PCR.…”

“…We performed clustering and network analyses on transcriptome data to identify key genes associated to its capacity to dehydrate and rehydrate. This work will contribute to the very limited information on gene discovery associated to desiccation tolerance in Hymenophyllaceae filmy ferns found in literature (Ostria-Gallardo et al, 2020).…”