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The Aquatic Resurrection Plant Chamaegigas Intrepidus – Adaptation to Multiple Abiotic Stresses and Habitat Isolation

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The Aquatic Resurrection Plant Chamaegigas Intrepidus – Adaptation to Multiple Abiotic Stresses and Habitat Isolation 38 (1): (2014) 69-80 Review Article The aquatic resurrection plant Chamaegigas intrepidus – adaptation to multiple abiotic stresses and habitat isolation Hermann Heilmeier1✳ and Wolfram Hartung2 1 Interdisciplinary Ecological Centre, TU Bergakademie Freiberg, Leipziger Str. 29, D-09599 Freiberg, Germany 2 Julius-von-Sachs-Institut für Biowissenschaften, Lehrstuhl Botanik I, Universität Würzburg, Julius-von-Sachs- Platz 2, D-97082 Würzburg, Germany ABSTRACT: Chamaegigas intrepidus is a tiny poikilohydrous member of the Linderniaceae growing endemically in ephemeral rock pools on granite outcrops in Central Namibia. Habitat conditions are characterised by (1) frequent and fast desiccation and rehydration during the rainy summer season, (2) complete dehydration during the dry winter season lasting up to 11 months, (3) intensive solar irradiation and high temperatures during the dry season, (4) diurnal oscillations of pH in the pool water up to 6 units, (5) extreme nutrient deficiencies, especially nitrogen. Anatomical, biochemical and physiological adaptations to this complex of extreme environmental conditions are discussed such as contractive xylem, accumulation of carbohydrates, dehydrins and abscisic acid during desiccation, and the role of amino acids, ammonium, urea and urease for nitrogen nutrition. Furthermore, Chamaegigas populations on single inselbergs are genetically isolated, whereas gene flow between sub-populations from different pools on one inselberg is rather high. This pattern of gene flow is discussed in the context of the breeding system of Ch. intrepidus. Key words: poikilohydrous cormophytes, limnology, desiccation, gene flow, Namibia Received: 23 January 2014 Revision accepted 03 March 2014 UDK 581.5(430.1) INTRODUCTION Poikilohydrous plant species can equilibrate their leaf tissues with air humidity down to 0% and can be Although desiccation-tolerant (poikilohydrous) angiosperms revived from this air-dried state (Gaff 1971). These comprise some 0.1% of all flowering plants only ‘resurrection plants’ usually grow as pioneer species (Porembski 2011), they have attracted the interest of on sites with very harsh environmental conditions, plant scientists for more than a century. The first botanist especially limited seasonal water availability, e.g. on rock to describe such species was the German taxonomist outcrops (Porembski 2011). Most of them are found in Kurt Dinter, who mentions four desiccation-tolerant (sub-)tropical Africa, Western Australia, India and South angiosperms (Chamaegigas intrepidus, Craterostigma America, and only a small number occurs in Northern and plantagineum, Myrothamnus flabellifolia and Xerophyta Central America and in Europe. Desiccation tolerance has viscosa) in his flora of South-West Africa (Dinter evolved within angiosperms independently several times, 1909). The most spectacular species among them is the both among monocotyledonous and dicotyledonous tiny Chamaegigas intrepidus Dinter, formerly Lindernia plants, but not in gymnosperms. intrepidus (Dinter) Oberm., a member of the Linderniaceae Resurrection plants within the dicotyledons are (formerly Scrophulariaceae) family, growing endemically mainly found within Gunnerales (Myrothamnaceae) and in Namibia. Lamiales (Gesneriaceae, Linderniaceae, Plantaginaceae). ✳correspondence: [email protected] © 2014 Institute of Botany and Botanical Garden Jevremovac, Belgrade 70 vol. 38 (1) Both Gesneriaceae and Linderniaceae contain more than description on the history of discovery of Ch. intrepidus can a dozen species. Some poikilohydrous members of the be found in Heilmeier & Hartung (2009). genus Lindernia and Ch. intrepidus colonize seasonally Chamaegigas is adapted to the fluctuations of wet water-filled rock pools (Porembski 2011). and dry conditions at its habitat through its ability for Chamaegigas intrepidus grows in shallow ephemeral fast de- and rehydration. When water from the pools rock pools on granite outcrops in Central Namibia (Fig. has been lost through evaporation, plants dry within less 1). Nearly 100 years ago, Kurt Dinter described the than two hours (Gaff & Giess 1986). After rewatering, extreme environmental conditions of the plant’s natural the vegetative organs regain full metabolic activity within habitat (Dinter 1918). Due to high temperature and a two hours (Hickel 1967). The extremely fast recovery high evaporative demand of the atmosphere the bottom after rehydration and the long survival in the desiccated of the pool in which he discovered this resurrection state make Chamaegigas by far the most impressive of plant remained permanently dry for at least half a year. all poikilohydrous angiosperms. In the following habitat During this time characterized by high solar irradiation, conditions and the plant’s mechanisms of adaptation to extreme temperatures and nearly completely dry air the its complex stressful environmental conditions at the plants survived as tiny rhizomes (diameter about 1 mm) anatomical, biochemical and physiological level will be and shrivelled leaves densely covering the bottom of the described as well as implications of its isolated geographical pool in a 1 cm thick layer of sand grains, dehydrated algae, distribution for generative reproduction and gene flow. dead daphnias, animal faeces and leaf litter. After the first summer rain falls had filled the small pools, a dense mat HABITUS, DiSTRIBUTION AND HABITAT of small green Chamaegigas leaves covered the bottom of the pools within minutes. After two days Dinter discovered Chamaegigas intrepidus is a small aquatic plant with two pink-coloured flowers in the midst of small rosette leaves types of leaves: (i) 8 - 15 mm long lanceolate submerged floating on the water on top of a thin stem. A detailed leaves on a short main axis, (ii) two decussate pairs of sessile Fig. 1. Temporarily water-filled rock pool at the end of the summer rainy period with Chamaegigas intrepidus on a granite outcrop on the farm Otjua (Omaruru District, Central Namibia) H. Heilmeier and W. Hartung: Stress adaptation in the aquatic resurrection plant Chamaegigas intrepidus 71 floating leaves which form a small rosette on top of the thin conditions, part of which are common for all resurrection stem which is attached to the main axis. The length of the plants (extremely severe edaphic drought and high solar stalk (1.5 to 10 cm) depends on the water level in the pools. irradiation concomitant with high air temperature and low Two flowers are produced in the rosette of the floating leaves air humidity during the dry season). The aquatic habitat, (Heil 1924). Their appearance is fully described in mookS however, exposes the plant to additional stressors, namely (1969) and Fischer (1992). The rhizome grows close to the recurrent flooding and drying cycles, low nutrient contents bottom of the pools and bears a dense mat of fine roots. and drastic diurnal fluctuations of pH of the water during All parts of the plant become totally dry when the the wet season. Furthermore the geographical isolation of rock pools dry out. Submerged and floating leaves get the inselbergs will limit gene flow affecting both genetic shrivelled. However, whereas mature floating leaves are differentiation between populations and genetic diversity considered desiccation-sensitive, immature floating leaves within populations. and submerged leaves are desiccation-tolerant (Gaff 1971). We investigated this complex set of multiple stressors Thus Ch. intrepidus is exceptional in possessing two types during several seasons in the natural habitat of Ch. of leaves with such a distinct contrast in drought tolerance intrepidus in Central Namibia (cf. Fig. 1 in Heilmeier et on the same plant. al. 2005). The research on ecophysiological adaptations to Chamaegigas grows endemically in Namibia (Fischer abiotic environmental factors was performed on the farm 1992), exclusively in areas with granite outcrops (inselbergs) Otjua, Omaruru District at a height of ca. 1400 m above see in the semi-desert and savanna transition zone (Giess 1969, level (for site description refer to Heilmeier & Hartung 1997). This arid to semi-arid region receives 160 to 570 mm 2001, 2011). precipitation per year, with rainfalls on only 20 to 70 days during summer (November to April), and a high variability The resurrection plant Chamaegigas: Anatomical, from year to year. A few (5 to 12) rainy days alternate with a physiological, biochemical and molecular adaptations number (up to 60) of dry days during the wet season (Hickel to desiccation and high irradiance stress. Like any 1967). During dry days the shallow rock pools (maximum resurrection plant, Ch. intrepidus is exposed to severe water level ca. 15 cm) usually dry out completely. In total, dehydration, concomitant with intensive insolation. This these ephemeral pools may be filled with water for some 40 combination of extreme environmental factors imposes to 85 days over the whole wet season. Thus the plant may three kinds of stress to the plants: (i) mechanical stress, experience 15 to 20 rehydration-dehydration cycles during (ii) destabilization and loss of integrity of supramolecular a single rainy season (Gaff & Giess 1986). Annual average structures like membranes, (iii) oxidative stress (Farrant temperature is 20 °C. However, air temperatures may 2000; Vicré et al. 2004a). rise up to 42 °C during the dry season, and sun-exposed rocks heat up to 50 °C at least (Dinter 1918). Average air Anatomical adaptations of leaves and roots. Hydrated humidity is 40%,
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