Resurrection Plants and Drought Tolerance
By: Farah Deeba and Vivek Pandey*
On a global basis, about one-third of potential arable land suffers from inadequate water supply, and the yields of much of the remainder are periodically reduced by drought. The responses at various levels are modulated by the intensity, duration, and rate of progression of imposed drought. Droughts have a wide range of effects on the masses in a developing country like India. The impact of droughts is specifically conspicuous in view of the tropical monsoon character of the country. Rainfall by the south-west monsoon is notorious for its vagaries. Indian agriculture still largely depends upon monsoon rainfall where about two-thirds of the arable land lack irrigation facilities and is termed as rain fed. The effect is manifested in the shortfalls of agricultural production in drought years. History is replete with examples of serious shortfall in cultivated areas and drop in agricultural productivity. It is worth mentioning that the shortfall in agricultural production may be the direct impact of meteorological droughts but the succeeding hydrological and agricultural droughts have a long range and far reaching impact on agriculture. Severe shortage of food-grains had been felt and the country had to resort to import of food-grains to save the poor people from hunger and starvation. However, India has been able to build a buffer stock of food–grains and threat from droughts is not as serious as it used to be before the Green Revolution. It is anticipated that yields from rain-fed farming in some south Asian countries could fall by up to 30% by 2050 (IPCC, 2007).
Under both natural and agricultural conditions, plants are frequently exposed to water stress. The phenomenon of desiccation tolerance is found throughout the microbial, fungal, animal and plant kingdoms. In the plant kingdom, it is mainly seeds and non-tracheophytes, such as mosses, that commonly display tolerance to desiccation. Almost every plant process is affected directly or indirectly by water stress. Water stress may range from moderate, and of short duration, to extremely severe and prolonged drought that strongly influence plant growth and function.
The physiological responses of plants to water stress and their relative importance for crop productivity vary with species, soil type, nutrients and climate. Plants perceive and respond rapidly to alterations (even small) in water status via a series of physiological, cellular, and molecular events developing in parallel. These events can contribute to coping with drought stress, either increasing its ability to avoid damage (avoidance mechanisms) and/or maintaining its metabolic functions under water limiting conditions (tolerance mechanisms). 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. Many mosses, lichens and ferns can survive dehydration of their vegetative organs, whereas this is uncommon in tracheophytes. Although there are no gymnosperms that show vegetative desiccation tolerance, there are several angiosperm families that contain desiccation-tolerant members. These individual species are collectively referred to as ‘resurrection plants’. Upon dehydration, resurrection plants shrivel up and fold their leaves until water is available, whereupon these plants revive in a remarkable manner. Plants adapt to drought by a number of physiological and morphological mechanisms. Leaf movements are common adaptive responses to drought stress in plants. One of these movements, leaf rolling is a hydronastic mechanism that reduces light interception, transpiration and leaf dehydration. In desiccation-tolerant plants also, curling or folding are the most obvious response to desiccation stress. The leaves of Xerophyta humilis are ﬂat and grass like. Upon dehydration the leaf blades fold in half along the midrib and only the abaxial surfaces are exposed to the light which is thought to serve to reduce light absorbed by the leaf in the desiccated state. In fully hydrated Craterostigma wilmsii plants, the leaves are green and expanded. As the plant dries, leaves progressively curl inward and become tightly folded with only the abaxial surfaces of the outer whorl of older leaves exposed to sunlight. It is thought that a number of morphological modiﬁcations associated with dehydration are adaptations of resurrection plants to minimize damage from light (and consequent free radical stress) in the dry tissues. Water loss is minimized by reducing light absorbance through rolled leaves. Immediate responses and slower adaptation responses can be distinguished. One of the ﬁrst physiological responses is stomatal closure, governed mainly by the plant hormone abscisic acid (ABA). Stomatal closure is modulated by a number of factors, including ion channels, protein kinases and phosphatases, lipid messengers, reactive oxygen species (ROS), and positive and negative transcriptional regulators. This is followed by down regulation of photosynthesis, which also serves to minimize ROS production. Osmoprotectants such as late embryogenesis abundant (LEA) proteins, polyols, proline, sucrose, and other sugars rapidly accumulate in many tissues. Aquaporins play an important role for water redistribution among different tissues and cellular compartments. Functional
antioxidant systems are also essential for protection against excessive ROS production under drought. Much slower responses include biochemical alterations in the cell wall and changes in root architecture. However, proliferation of the root system in response to water deﬁcit is often coupled with reduced above-ground plant growth. Signalling events that lead to these responses involve activation of ion channels, Na+/H+ antiporters, Ca2+-binding proteins such as calmodulin and calcium-dependent protein kinases, receptor-like kinases, and mitogen activated protein kinases. These early signalling events eventually regulate transcriptional factors and coregulators that govern the global transcriptional re-programming necessary for the execution of the above-mentioned physiological and morphological changes, resulting in adjustment to drought stress.
Several resurrection plant species, including Myrothamnus flabellifolia, Craterostigma plantagineum, Craterostigma wilmsii, Xerophyta viscosa, Xerophyta humilis, Eragrostis nindensis and Sporobolus stapfianus, have been intensively studied with the goal of identifying the mechanisms responsible for their remarkable desiccation tolerance. 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. Research on desiccation tolerance has generally been conducted using discipline-specific approaches, focusing exclusively on the physiological, metabolic, molecular, genetic, biochemical or ultrastructural changes that occur in resurrection plants during dehydration and rehydration. 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.
Resurrection plants: Overview
Resurrection plants are unique in that they are able to lose more than 95 % of the water in vegetative tissues, fall into anabiosis for long periods, and regain full functions after rehydration. Vegetative desiccation tolerance is more common in lower plants such as bryophytes, rare in pteridophytes and angiosperms, and absent in gymnosperms. It has been estimated that the total number of desiccation-tolerant plants is at least c. 1,300 (1,000 pter-idophytes and 300 angiosperm plants). While the mechanisms of desiccation tolerance in bryophytes are mainly related to cellular repair, the more complex tissues in angiosperms require mechanisms that prevent desiccation-induced cell- and tissue damage in the ﬁrst place.
The small group of angiosperm resurrection plants displays remarkable habitat and geographic diversity throughout both the northern and the southern hemispheres. Resurrection plants can be found among both monocots and dicots. Most occur in dry and desert areas or in more temperate areas with sufficient rain precipitation but periods of drought or/and cold winters (like the European resurrection plants Haberlea rhodopensis and Ramonda serbica). A resurrection plant, Lindernia brevidens, was even discovered in the tropical rainforests of Africa, where humidity is always high. Most of the resurrection species are herbaceous plants.
The resurrection plants are interesting not only because of the desiccation tolerance and as a source for gene discovery but also because they have unique metabolites, some of which have potential uses in biotechnology and medicine. For example, the South African woody resurrection species Myrothamnus ﬂabellifolia has long been known for its medicinal properties. Its extracts, rich in polyphenols and essential oils, are used to treat various disorders, including inﬂuenza, kidney diseases, and gingivitis. The predominant polyphenol 3,4,5-tri-O-galloylquinic acid has been shown to inhibit M-MLV and HIV-1 reverse transcriptases. Myconoside, a glycoside abundantly present in extracts of H. rhodopensis, can strongly stimulate antioxidant skin defenses and extracellular matrix protein synthesis. Extracts from H. rhodopensis, which are also rich in polyphenols, can stimulate the synthesis of elastin in a dose-dependent manner and also possess radioprotective, anticlastogenic, and antioxidant effects on rabbit blood samples exposed to gamma radiation in vitro. These results suggest that the strong medicinal properties of some resurrection plants should be the aim of further extensive experiments which could provide strategies and solutions in combating various human diseases.
Resurrection plants are interesting potential sources for desiccation tolerant genes to be used in crop improvement. Furthermore, using a systems biology approach (transcriptomics, genomics, proteomics, metabolomics) 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 economic crop species.
*Plant Physiology Laboratory, CSIR-NBRI, Rana Pratap Marg, Lucknow-226001, India.