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Key messageCell wall plasticity plays a very crucial role in vegetative and reproductive development of rice under drought and is a highly potential trait for improving rice yield under drought.Drought is a major constraint in rice (Oryza sativa L.) cultivation severely affecting all developmental stages, with the reproductive stage being the most sensitive. Rice plants employ multiple strategies to cope with drought, in which modification in cell wall dynamics plays a crucial role. Over the years, significant progress has been made in discovering the cell wall-specific genomic resources related to drought tolerance at vegetative and reproductive stages of rice. However, questions remain about how the drought-induced changes in cell wall made by these genomic resources potentially influence the vegetative and reproductive development of rice. The possibly major candidate genes underlying the function of quantitative trait loci directly or indirectly associated with the cell wall plasticization-mediated drought tolerance of rice might have a huge promise in dissecting the putative genomic regions associated with cell wall plasticity under drought. Furthermore, engineering the drought tolerance of rice using cell wall-related genes from resurrection plants may have huge prospects for rice yield improvement. Here, we review the comprehensive multidisciplinary analyses to unravel different components and mechanisms involved in drought-induced cell wall plasticity at vegetative and reproductive stages that could be targeted for improving rice yield under drought.

Plant species that exhibit vegetative desiccation tolerance can survive extreme desiccation for months and resume normal physiological activities upon re-watering. Here we survey the recent knowledge gathered from the sequenced genomes of angiosperm and non-angiosperm desiccation-tolerant plants (resurrection plants) and highlight some distinct genes and gene families that are central to the desiccation response. Furthermore, we review the vast amount of data accumulated from analyses of transcriptomes and metabolomes of resurrection species exposed to desiccation and subsequent rehydration, which allows us to build a systems biology view on the molecular and genetic mechanisms of desiccation tolerance in plants.

Aims and background The resurrection plant Myrothamnus flabellifolia tolerates complete desiccation and is a great model for studying how plants cope with extreme drought. Root-associated microbes play a major role in stress tolerance and are an attractive target for enhancing drought tolerance in staple crops. However, how these dynamics play out under the most extreme water limitation remains underexplored. This study aimed to identify bacterial and fungal communities that tolerate extreme drought stress in the bulk soil, rhizosphere, and endosphere of M. flabellifolia . Methods High-throughput amplicon sequencing was used to characterise the microbial communities associated with M. flabellifolia . Results The bacterial phyla that were most abundant across all compartments were Acidobacteriota, Actinobacteriota, Chloroflexota, Planctomycetota, and Pseudomonadota , while the most abundant fungal phyla were Ascomycota and Basidiomycota . Although the bulk soil hosted multiple beneficial root-associated microbes, the rhizosphere compartment showed the highest functional diversity of bacteria and fungi. In contrast, the endosphere exhibited a low abundance and diversity of microbes. These findings share consistent with the theory that M. flabellifolia recruits soil microbes from the bulk to the rhizosphere and finally to the endosphere. It is possible that these microbes could promote drought tolerance in associated plant tissues. Conclusion We find that compartments act as the major driver of microbial diversity, but the soil physicochemical factors also influence microbial composition. These results suggest that the root-associated microbiome of M. flabellifolia is highly structured and may aid in plant function.

Although staple crops do not survive extended periods of drought, their seeds possess desiccation tolerance (DT), as they survive almost complete dehydration (desiccation) during the late maturation phase of development. Resurrection plants are plant species whose seeds and vegetative tissues are desiccation tolerant. Vegetative DT first arose with the transition from aquatic to terrestrial life forms, but it was lost as plants acquired mechanisms for drought resistance. DT was then confined to seeds, spores, and pollen grains. We review evidence suggesting that angiosperm resurrection plants have reactivated the seed DT program in vegetative tissues. Novel omics technologies are providing a better understanding of the changes necessary for this reactivation and may aid in the development of crop varieties that are better able to survive extreme drought conditions.

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 well-defined 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.

A variety of Southern African resurrection plants were surveyed using high-throughput cell wall profiling tools. Species evaluated were the dicotyledons, Myrothamnus flabellifolia and Craterostigma plantagineum; the monocotyledons, Xerophyta viscosa, Xerophyta schlecterii, Xerophyta humilis and the resurrection grass Eragrostis nindensis, as well as a pteridophyte, the resurrection fern, Mohria caffrorum. Comparisons were made between hydrated and desiccated leaf and frond material, with respect to cell wall composition and polymer abundance, using monosaccharide composition analysis, FT-IR spectroscopy and comprehensive microarray polymer profiling in combination with multivariate data analysis. The data obtained suggest that three main functional strategies appear to have evolved to prepare plant cell walls for desiccation. Arabinan-rich pectin and arabinogalactan proteins are found in the resurrection fern M. caffrorum and the basal angiosperm M. flabellifolia where they appear to act as 'pectic plasticizers'. Dicotyledons with pectin-rich walls, such as C. plantagineum, seem to use inducible mechanisms which consist of up-regulating wall proteins and osmoprotectants. The hemicellulose-rich walls of the grass-like Xerophyta spp. and the resurrection grass E. nindensis were found to contain highly arabinosylated xylans and arabinogalactan proteins. These data support a general mechanism of 'plasticising' the cell walls of resurrection plants to desiccation and implicate arabinose-rich polymers (pectin-arabinans, arabinogalactan proteins and arabinoxylans) as the major contributors in ensuring flexibility is maintained and rehydration is facilitated in these plants.

Haberlea rhodopensis is a resurrection plant with remarkable tolerance to desiccation. Haberlea exposed to drought stress, desiccation, and subsequent rehydration showed no signs of damage or severe oxidative stress compared to untreated control plants. Transcriptome analysis by next-generation sequencing revealed a drought-induced reprogramming, which redirected resources from growth towards cell protection. Repression of photosynthetic and growth-related genes during water deficiency was concomitant with induction of transcription factors (members of the NAC, NF-YA, MADS box, HSF, GRAS, and WRKY families) presumably acting as master switches of the genetic reprogramming, as well as with an upregulation of genes related to sugar metabolism, signaling, and genes encoding early light-inducible (ELIP), late embryogenesis abundant (LEA), and heat shock (HSP) proteins. At the same time, genes encoding other LEA, HSP, and stress protective proteins were constitutively expressed at high levels even in unstressed controls. Genes normally involved in tolerance to salinity, chilling, and pathogens were also highly induced, suggesting a possible cross-tolerance against a number of abiotic and biotic stress factors. A notable percentage of the genes highly regulated in dehydration and subsequent rehydration were novel, with no sequence homology to genes from other plant genomes. Additionally, an extensive antioxidant gene network was identified with several gene families possessing a greater number of antioxidant genes than most other species with sequenced genomes. Two of the transcripts most abundant during all conditions encoded catalases and five more catalases were induced in water-deficient samples. Using the pharmacological inhibitor 3-aminotriazole (AT) to compromise catalase activity resulted in increased sensitivity to desiccation. Metabolome analysis by GC or LC–MS revealed accumulation of sucrose, verbascose, spermidine, and γ-aminobutyric acid during drought, as well as particular secondary metabolites accumulating during rehydration. This observation, together with the complex antioxidant system and the constitutive expression of stress protective genes suggests that both constitutive and inducible mechanisms contribute to the extreme desiccation tolerance of H. rhodopensis .

The genome analysis presented here represents a major step forward in the field of desiccation tolerance and a much-anticipated resource that will have a far-reaching effect in many areas of plant biology and agriculture. We present the ∼1.69-Gb draft genome of Boea hygrometrica , an important plant model for understanding responses to dehydration. To our knowledge, this is the first genome sequence of a desiccation-tolerant extremophile, offering insight into the evolution of this important trait and a first look, to our knowledge, into the genome organization of desiccation tolerance. The underpinning genome architecture and response in relation to the hydration state of the plant and its role in the preservation of cellular integrity has important implications for developing drought tolerance improvement strategies for our crops. “Drying without dying” is an essential trait in land plant evolution. Unraveling how a unique group of angiosperms, the Resurrection Plants, survive desiccation of their leaves and roots has been hampered by the lack of a foundational genome perspective. Here we report the ∼1,691-Mb sequenced genome of Boea hygrometrica , an important resurrection plant model. The sequence revealed evidence for two historical genome-wide duplication events, a compliment of 49,374 protein-coding genes, 29.15% of which are unique (orphan) to Boea and 20% of which (9,888) significantly respond to desiccation at the transcript level. Expansion of early light-inducible protein (ELIP) and 5S rRNA genes highlights the importance of the protection of the photosynthetic apparatus during drying and the rapid resumption of protein synthesis in the resurrection capability of Boea . Transcriptome analysis reveals extensive alternative splicing of transcripts and a focus on cellular protection strategies. The lack of desiccation tolerance-specific genome organizational features suggests the resurrection phenotype evolved mainly by an alteration in the control of dehydration response genes.

Ramonda serbica Panc. is an ancient resurrection plant able to survive a long desiccation period and recover metabolic functions upon watering. The accumulation of protective late embryogenesis abundant proteins (LEAPs) is a desiccation tolerance hallmark. To propose their role in R. serbica desiccation tolerance, we structurally characterised LEAPs and evaluated LEA gene expression levels in hydrated and desiccated leaves. By integrating de novo transcriptomics and homologues LEAP domains, 318 R. serbica LEAPs were identified and classified according to their conserved motifs and phylogeny. The in silico analysis revealed that hydrophilic LEA4 proteins exhibited an exceptionally high tendency to form amphipathic α-helices. The most abundant, atypical LEA2 group contained more hydrophobic proteins predicted to fold into the defined globular domains. Within the desiccation-upregulated LEA genes, the majority encoded highly disordered DEH1, LEA1, LEA4.2, and LEA4.3 proteins, while the greatest portion of downregulated genes encoded LEA2.3 and LEA2.5 proteins. While dehydrins might chelate metals and bind DNA under water deficit, other intrinsically disordered LEAPs might participate in forming intracellular proteinaceous condensates or adopt amphipathic α-helical conformation, enabling them to stabilise desiccation-sensitive proteins and membranes. This comprehensive LEAPs structural characterisation is essential to understanding their function and regulation during desiccation aiming at crop drought tolerance improvement.

Background Understanding the response of resurrection angiosperms to dehydration and rehydration is critical for deciphering the mechanisms of how plants cope with the rigors of water loss from their vegetative tissues. We have focused our studies on the C 4 resurrection grass, Sporobolus stapfianus Gandoger, as a member of a group of important forage grasses. Methods We have combined non-targeted metabolomics with transcriptomics, via a NimbleGen array platform, to develop an understanding of how gene expression and metabolite profiles can be linked to generate a more detailed mechanistic appreciation of the cellular response to both desiccation and rehydration. Results The rehydration transcriptome and metabolome are primarily geared towards the rapid return of photosynthesis, energy metabolism, protein turnover, and protein synthesis during the rehydration phase. However, there are some metabolites associated with ROS protection that remain elevated during rehydration, most notably the tocopherols. The analysis of the dehydration transcriptome reveals a strong concordance between transcript abundance and the associated metabolite abundance reported earlier, but only in responses that are directly related to cellular protection during dehydration: carbohydrate metabolism and redox homeostasis. The transcriptome response also provides strong support for the involvement of cellular protection processes as exemplified by the increases in the abundance of transcripts encoding late embryogenesis abundant (LEA) proteins, anti-oxidant enzymes, early light-induced proteins (ELIP) proteins, and cell-wall modification enzymes. There is little concordance between transcript and metabolite abundance for processes such as amino acid metabolism that do not appear to contribute directly to cellular protection, but are nonetheless important for the desiccation tolerant phenotype of S. stapfianus . Conclusions The transcriptomes of both dehydration and rehydration offer insight into the complexity of the regulation of responses to these processes that involve complex signaling pathways and associated transcription factors. ABA appears to be important in the control of gene expression in both the latter stages of the dehydration and the early stages of rehydration. These findings add to the growing body of information detailing how plants tolerate and survive the severe cellular perturbations of dehydration, desiccation, and rehydration.