Jill M. Farrant

Desiccation tolerance in resurrection plants

The phenomenon of desiccation tolerance is found throughout the microbial, fungal, animal and plant kingdoms [1,2]. In the plant kingdom, it is mainly seeds and non-tracheophytes, such as mosses, that commonly display tolerance to desiccation [3]. Desiccation tolerance, as opposed to drought tolerance, which involves surviving moderate water loss (e.g. 90% relative water content [RWC]), is the ability to survive absolute water contents of 0.1 g H2O g1 [2].

Most seeds are termed ‘orthodox’ because they can survive dehydration to an air-dry state, whereas a minority is called ‘recalcitrant’ because they show a marked sensitivity to such severe dehydration [4]. Many mosses, lichens and ferns can survive dehydration of their vegetative organs (e.g. leaves), whereas this is uncommon in tracheophytes [3,5,6]. Although there are no gymnosperms that show vegetative desiccation tolerance, there are several angiosperm families that contain desiccation-tolerant members [3]. These individual species are collectively referred to as ‘resurrection plants’ [7]. Upon dehydration, resurrection plants shrivel up and fold their leaves until water is available, whereupon these plants revive in a remarkable manner (see Online Supplementary Movies showing resurrection plants rehydrating). A rich diversity of resurrection plants is found in southern Africa, a region of significant arid and semi-arid areas [7]. Several species, including Myrothamnus flabellifolia [8], Craterostigma plantagineum [9], Craterostigma wilmsii [10], Xerophyta viscosa [11], Xerophyta humilis [12], Eragrostis nindensis [13] and Sporobolus stapfianus [14,15] (Figure 1), have been intensively studied with the goal of identifying the mechanisms responsible for their remarkable tolerance (Figure 1). Desiccation tolerance seems to not necessarily require the presence of novel molecular structures; however, the developmentally triggered re-activation of established pathways and processes seems to be crucial in conferring tolerance [2,9]. Research on desiccation tolerance has generally been conducted using discipline-specific approaches, focusing exclusively on the physiological [16,17], metabolic [15], molecular genetic [14,18], biochemical [19,20] or ultrastructural [21] changes that occur in resurrection plants during dehydration and rehydration. Although such research has been responsible for significant advances in our understanding of desiccation tolerance, disciplinespecific approaches suffer because the process under study is inherently complex and requires cross-disciplinary investigations to link the various concepts related to tolerance into a coherent whole. Here, we present major recent advances made through studying a variety of different aspects that seem to be important for resurrection plants to be able to survive desiccation. These include gene regulation networks and signal transduction pathways [9,14], compatible solutes and carbohydrate metabolism [15,22], desiccation-associated proteins [19,23], conventional and novel antioxidants [20,24,25], membrane protectants [20] and cell wall properties [21,26–28].We believe that, for tolerance to emerge, these fundamental processes, constituting cellular information regulation, energy metabolism and structural organization, must be integrated through coordinated metabolic and signaling events. Furthermore, we propose that using a systemsbiology approach will lead to a significantly improved understanding of the mechanisms associated with plant desiccation tolerance. This is important for improving the application of genetic-engineering approaches in enhancing drought tolerance in valuable crop species, such as maize (Zea mays) and grapevine (Vitis vinifera).

Extract from: Towards a systems-based understanding of plant desiccation tolerance

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