Jill M. Farrant

The evolution of resurrection plants

All modified-desiccation tolerant plants are seed plants and therefore seeds are likely to be the source of genetic programming for the evolution of all angiosperm resurrection plants [2]. Different desiccation-tolerant resurrection plant lineages exist and therefore, acquisition of ‘seed’ DT must have occurred multiple times during angiosperm evolution. Owing to the lack of a fully sequenced resurrection plant genome transcriptomic studies have been limited to the analysis of expressed sequence tags (EST) [17]. Microarray and small-scale sequence cDNA analysis has been performed on a number of species, including, Tortula ruralis [5], Selaginella lepidophylla [32], Xerophyta humilis [33], Myrothamnus flabellifolia [34], Sporobolus stapfianus [35] and Craterostigma plantagineum [36]. Figure 1 shows all these species in the hydrated state. The most comprehensive transcriptomic analysis of a resurrection plant has recently been performed for C. plantagineum using pyro-sequencing technology [37]. Four cDNA libraries were constructed from fully hydrated, 48 h dehydrated, 15 day dehydrated and 24 h rehydrated leaf tissue of C. plantagineum. After sequence assembly over 15,000 UniProt identities were obtained, the highest coverage to date for any resurrection plant. The 500 most variable transcripts, across all experimental samples, were partition clustered and subjected to functional enrichment analysis. Gene ontology (GO) categories enriched within the six expression clusters included responses to abiotic stimuli such as ABA, stress response pathways, oxidative processes, antioxidant responses to oxidative metabolism, cellular polysaccharide metabolism and cell wall organization, and photosynthesis and cytoskeletal organization. This study confirmed the results of many previous molecular studies of DT in this species and others; re-enforcing the importance of LEAs, sugars, antioxidants and cell wall genes encoding expansins and xyloglucan endotransglucosylases during desiccation [12,13,38]. One interesting observation from the data is the many chromosome scaffold genes are responsive to desiccation and one hypothesis is that C. plantagineum has evolved proteins aiding the recruitment of transcripts to histone complexes during desiccation and thus utilizes a similar strategy of mRNP production to that of Tortula ruralis [37]. However we know that the DT of T. ruralis is a constitutive repair strategy that is metabolically expensive. By contrast, DT in C. plantagineum probably evolved from a developmental- seed program that was ‘re-activated’ to respond to environmental cues. A molecular ‘signature of seeds’ in resurrection plants, however, has not yet been convincingly demonstrated [18]. One molecular study, currently unpublished, has produced data that strongly supports the seed origin of the DT genetic program in angiosperm resurrection plants [39]. It was reasoned that one approach to prove the seed origin was to compare gene expression of desiccated vegetative tissue with mature dry seed material sourced from a resurrection plant. A control parallel experiment involving use of a desiccationsensitive plant in order to compare water stressed vegetative tissue with its corresponding mature seed transcriptome was included. In addition to profiling for potential new pathways, this approach could identify pathways common to desiccated vegetative tissue and mature dry seeds. This experiment was carried out using Xerophyta humilis, a resurrection plant (Figure 1D), and Arabidopsis thaliana, the desiccation sensitive control, using cDNA and Microarray technology [39]. Of the X. humilis genes analyzed, 46% were found to be differentially expressed between seed and desiccated vegetative tissue. Cluster analysis and multivariate techniques revealed that the transcriptomes of desiccated root, desiccated leaf and seed tissue were very similar to each other in X. humilis. This is in contrast to A. thaliana where there is no clear overlap between gene expression clusters of stressed vegetative tissue and seed tissue, indicating that the response to water stress is tissue specific in A. thaliana. Of particular interest was the identification of a common set of genes in X. humilis, encoding LEAs, HSPs, peroxiredoxins and storage proteins, that were expressed in roots, leaves and seeds of desiccated X. humilis, but are seed-specific in A. thaliana (according to TAIR annotation). The overall conclusions from this study are that desiccation tolerant angiosperms, such as X. humilis and C. plantagineum, utilize a seed-specific developmental program that is ‘re-activated’ in vegetative tissues to protect against desiccation.


Extract from: Programming desiccation-tolerance: from plants to seeds to resurrection plants

You are here: