Although several resurrection plant genomes have been sequenced, the lack of suitable dehydration-sensitive outgroups has limited genomic insights into the origin of desiccation tolerance. Here, we utilized a comparative system of closely related desiccation-tolerant (Lindernia brevidens) and -sensitive (Lindernia subracemosa) species to identify gene-and pathwaylevel changes associated with the evolution of desiccation tolerance. The two high-quality Lindernia genomes we assembled are largely collinear, and over 90% of genes are conserved. L. brevidens and L. subracemosa have evidence of an ancient, shared whole-genome duplication event, and retained genes have neofunctionalized, with desiccation-specific expression in L. brevidens. Tandem gene duplicates also are enriched in desiccation-associated functions, including a dramatic expansion of early light-induced proteins from 4 to 26 copies in L. brevidens. A comparative differential gene coexpression analysis between L. brevidens and L. subracemosa supports extensive network rewiring across early dehydration, desiccation, and rehydration time courses. Many LATE EMBRYOGENESIS ABUNDANT genes show significantly higher expression in L. brevidens compared with their orthologs in L. subracemosa. Coexpression modules uniquely upregulated during desiccation in L. brevidens are enriched with seed-specific and abscisic acid-associated cis-regulatory elements. These modules contain a wide array of seed-associated genes that have no expression in the desiccation-sensitive L. subracemosa. Together, these findings suggest that desiccation tolerance evolved through a combination of gene duplications and network-level rewiring of existing seed desiccation pathways.
Summary The resurrection plant Craterostigma plantagineum possesses an extraordinary capacity to survive long‐term desiccation. To enhance our understanding of this phenomenon, complementary transcriptome, soluble proteome and targeted metabolite profiling was carried out on leaves collected from different stages during a dehydration and rehydration cycle. A total of 7348 contigs, 611 proteins and 39 metabolites were differentially abundant across the different sampling points. Dynamic changes in transcript, protein and metabolite levels revealed a unique signature characterizing each stage. An overall low correlation between transcript and protein abundance suggests a prominent role for post‐transcriptional modification in metabolic reprogramming to prepare plants for desiccation and recovery. The integrative analysis of all three data sets was performed with an emphasis on photosynthesis, photorespiration, energy metabolism and amino acid metabolism. The results revealed a set of precise changes that modulate primary metabolism to confer plasticity to metabolic pathways, thus optimizing plant performance under stress. The maintenance of cyclic electron flow and photorespiration, and the switch from C3 to crassulacean acid metabolism photosynthesis, may contribute to partially sustain photosynthesis and minimize oxidative damage during dehydration. Transcripts with a delayed translation, ATP‐independent bypasses, alternative respiratory pathway and 4‐aminobutyric acid shunt may all play a role in energy management, together conferring bioenergetic advantages to meet energy demands upon rehydration. This study provides a high‐resolution map of the changes occurring in primary metabolism during dehydration and rehydration and enriches our understanding of the molecular mechanisms underpinning plant desiccation tolerance. The data sets provided here will ultimately inspire biotechnological strategies for drought tolerance improvement in crops.
Summary Craterostigma plantagineum tolerates extreme desiccation. Leaves of this plant shrink and extensively fold during dehydration and expand again during rehydration, preserving their structural integrity. Genes were analysed that may participate in the reversible folding mechanism. Analysis of transcripts abundantly expressed in desiccated leaves identified a gene putatively coding for an apoplastic glycine‐rich protein (CpGRP1). We studied the expression, regulation and subcellular localization of CpGRP1 and its ability to interact with a cell wall‐associated protein kinase (CpWAK1) to understand the role of CpGRP1 in the cell wall during dehydration. The CpGRP1 protein accumulates in the apoplast of desiccated leaves. Analysis of the promoter revealed that the gene expression is mainly regulated at the transcriptional level, is independent of abscisic acid (ABA) and involves a drought‐responsive cis‐element (DRE). CpGRP1 interacts with CpWAK1 which is down‐regulated in response to dehydration. Our data suggest a role of the CpGRP1–CpWAK1 complex in dehydration‐induced morphological changes in the cell wall during dehydration in C. plantagineum. Cell wall pectins and dehydration‐induced pectin modifications are predicted to be involved in the activity of the CpGRP1–CpWAK1 complex.
Summary Craterostigma plantagineum belongs to the desiccation‐tolerant angiosperm plants. Upon dehydration, leaves fold and the cells shrink which is reversed during rehydration. To understand this process changes in cell wall pectin composition, and the role of the apoplastic glycine‐rich protein 1 (CpGRP1) were analysed. Cellular microstructural changes in hydrated, desiccated and rehydrated leaf sections were analysed using scanning electron microscopy. Pectin composition in different cell wall fractions was analysed with monoclonal antibodies against homogalacturonan, rhamnogalacturonan I, rhamnogalacturonan II and hemicellulose epitopes. Our data demonstrate changes in pectin composition during dehydration/rehydration which is suggested to affect cell wall properties. Homogalacturonan was less methylesterified upon desiccation and changes were also demonstrated in the detection of rhamnogalacturonan I, rhamnogalacturonan II and hemicelluloses. CpGRP1 seems to have a central role in cell adaptations to water deficit, as it interacts with pectin through a cluster of arginine residues and de‐methylesterified pectin presents more binding sites for the protein−pectin interaction than to pectin from hydrated leaves. CpGRP1 can also bind phosphatidic acid (PA) and cardiolipin. The binding of CpGRP1 to pectin appears to be dependent on the pectin methylesterification status and it has a higher affinity to pectin than its binding partner CpWAK1. It is hypothesised that changes in pectin composition are sensed by the CpGRP1−CpWAK1 complex therefore leading to the activation of dehydration‐related responses and leaf folding. PA might participate in the modulation of CpGRP1 activity.
Taxonomically restricted genes are known to contribute to the evolution of new traits. In Craterostigma plantagineum two of such genes are modulated during dehydration and rehydration and seem to contribute to a successful recovery after desiccation. The resurrection plant Craterostigma plantagineum can tolerate extreme water loss. Protective molecules linked to desiccation tolerance were identified in C. plantagineum but underlying mechanisms are far from being completely understood. A transcriptome analysis revealed several genes which could not be annotated and are, therefore, interesting candidates for understanding desiccation tolerance. Genes which occur only in some species are defined as orphan or taxonomically restricted genes (TRGs) and may be important for the evolution of new traits. Several of these TRGs are modulated in expression during dehydration/rehydration in C. plantagineum. Here we report the characterisation of two of these TRGs encoding a cysteine-rich rehydration-responsive protein 1 (CpCRP1) and an early dehydration-responsive protein 1 (CpEDR1). The involvement of CpCRP1 and CpEDR1 in different phases of the dehydration/rehydration cycle is shown by transcript and protein expression analysis. In silico sequence analyses predicted that both genes are likely to interact with other cellular components and are localised in two different cellular compartments. GFP fusion proteins demonstrated that CpCRP1 is secreted into the apoplasm, whereas CpEDR1 is imported into chloroplasts. Putative homologs of CpCRP1 and CpEDR1 were identified in Lindernia brevidens and Lindernia subracemosa which belong to the same family as C. plantagineum thus suggesting a recent evolution of the genes in this family. According to expression profiles, CpCRP1 may play a role in normal conditions and during rehydration, whereas CpEDR1 may be required for the acquisition of desiccation tolerance and protect photosynthetic structures during dehydration and rehydration.
Plant cell walls define the shape of the cells and provide mechanical support. They function as osmoregulators by controlling the transport of molecules between cells and provide transport pathways within the plant. These diverse functions require a welldefined and flexible organization of cell wall components, i.e., water, polysaccharides, proteins, and other diverse substances. Cell walls of desiccation tolerant resurrection plants withstand extreme mechanical stress during complete dehydration and rehydration. Adaptation to the changing water status of the plant plays a crucial role during this process. This review summarizes the compositional and structural variations, signal transduction and changes of gene expression which occur in cell walls of resurrection plants during dehydration and rehydration.
The desiccation transcriptome of the resurrection plant C. plantagineum is composed of conserved protein coding transcripts, taxonomically restricted transcripts and recently evolved non-protein coding transcripts. Research in resurrection plants has been hampered by the lack of genome sequence information, but recently introduced sequencing technologies overcome this limitation partially and provide access to the transcriptome of these plants. Transcriptome studies showed that mechanisms involved in desiccation tolerance are conserved in resurrection plants, seeds and pollen. The accumulation of protective molecules such as sugars and LEA proteins are major components in desiccation tolerance. Leaf folding, chloroplast protection and protection during rehydration must involve specific molecular mechanisms, but the basis of such mechanisms is mainly unknown. The study of regulatory regions of a desiccation-induced C. plantagineum gene suggests that cis-regulatory elements may be responsible for expression variations in desiccation tolerant and non-desiccation-tolerant plants. The analysis of the C. plantagineum transcriptome also revealed that part of it is composed of taxonomically restricted genes (TRGs) and non-protein coding RNAs (ncRNAs). TRGs are known to code for new traits required for the adaptation of organisms to particular environmental conditions. Thus the study of TRGs from resurrection plants should reveal species-specific functions related to the desiccation tolerance phenotype. Non-protein coding RNAs can regulate gene expression at epigenetic, transcriptional and post-transcriptional level and thus these RNAs may be key players in the rewiring of regulatory networks of desiccation-related genes in C. plantagineum.
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