Unravelling the molecular network of desiccation tolerance in resurrection plants started with the model plant Craterostigma plantagineum

Abstract

Molecular studies of desiccation-tolerant resurrection plants identified major components for surviving severe water depletion of vegetative tissues. The research also highlights potential applications for crop protection during drought. The ability of vegetative plant tissues to withstand desiccation is a property of a small group of resurrection plants specific to specialized ecological niches. In the 1980s, studies on these plants were limited to the physiological and morphological levels. However, in 1990, a study by Bartels et al. using the South African resurrection plant Craterostigma plantagineum was the first to address desiccation tolerance at the molecular level. A differential screening approach with C. plantagineum leaves and callus pretreated with ABA led to the identification of transcripts that were upregulated by desiccation. Many of the identified genes encoded late embryogenesis-abundant (LEA) proteins, which are abundant proteins that accumulate during normal seed development. Therefore, the study confirmed that the acquisition of desiccation tolerance in vegetative tissues of resurrection plants partially involves the seed maturation programme involving ABA. Subsequent research with C. plantagineum contributed to elucidating the gene regulatory networks and metabolic changes that contribute to desiccation tolerance and provided the basis for studies with other resurrection species. More recently, the genomes of C. plantagineum and several other resurrection plants have been sequenced, which has allowed comparative genomics approaches to identify conserved mechanisms and signatures associated with vegetative desiccation tolerance. A primary goal remains to transfer existing knowledge from resurrection plants to genetically engineer drought tolerance in crop plants, which will improve survival during periods of drought and will maintain future food security despite increasing impacts of climate change.

Keywords: Abscisic acid; Evolution of desiccation; LEA proteins; Seed desiccation tolerance; Vegetative desiccation tolerance.

Fig. 1

Desiccation tolerance in Craterostigma plantagineum. a Acquisition of desiccation tolerance in Craterostigma plantagineum plants and dicot seeds. Upper panel: In dehydration–rehydration experiments, well-watered whole plants or detached leaves are air-dried until complete desiccation, during which more than 90% of water is lost. Plants can remain desiccated for several days or even months and restore full metabolic activities within 48 h upon rewatering. Lower panel: cartoon of a dicot seed during early and late embryogenesis phases when maturation involves the acquisition of desiccation tolerance. b Study of desiccation tolerance in Craterostigma plantagineum callus. Callus of C. plantagineum is sensitive to rapid desiccation, and cells cannot restore their metabolic activities upon dehydration and rehydration. However, treatment with the hormone ABA (5 mg L^-1) for 4 days induces desiccation tolerance. Only callus pretreated with ABA can rehydrate and proliferate when transferred to plates with nutrient medium

Fig. 2

Major breakthroughs in the study of desiccation tolerance in Craterostigma and other resurrection plants. The study of desiccation tolerance (DT) in plants gained momentum in the early 1970s. Initial research focussed on the physiology and metabolism of resurrection plants and how metabolites that accumulate upon dehydration protect these plants from damage. The study by Bartels et al. (1990) was the first to report molecular analyses of resurrection plants, identifying genes expressed in desiccation-tolerant tissues and introducing callus as a model system. One major discovery was the identification of key regulatory components, such as CDT-1. Advancements in understanding desiccation tolerance continued when genome sequences of resurrection plants became available. These genomic data and other omics data allowed systemic and large-scale comparative analyses. Today, genomic insights combined with gene-editing technologies can now help to validate hypotheses in resurrection plants and will potentially allow the transfer of knowledge to desiccation-sensitive (DS) plants. ¹Bartels et al. (1988); ²Koster and Leopold (1988); ³Gaff (1971); ⁴Gaff (1977); ⁵Schwab et al. (1989); ⁶Crowe et al. (1984); ⁷Schwab and Heber (1984); ⁸Bianchi et al. (1991); ⁹Leopold (1986); ¹⁰Bartels et al. (1990); ¹¹Furini et al. (1997); ¹²Velasco et al. (1998); ¹³Bartels et al. (2007); ¹⁴Gasulla et al. (2013); ¹⁵Moore et al. (2013); ¹⁶Rodriguez et al. (2010); ¹⁷Xu et al. (2021); ¹⁸VanBuren et al. (2023); ¹⁹VanBuren et al. (2015); ²⁰Xiao et al. (2015); ²¹Costa et al. (2017); ²²VanBuren et al. (2017); ²³Pardo et al. (2020); ²⁴Giarola et al. (2018); ²⁵VanBuren et al. (2018); ²⁶Jung et al. (2019)