Ecophysiological responses of homoiochlorophyllous and ...

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Plant Growth Regulation 24: 211–217, 1998. c 1998 Kluwer Academic Publishers. Printed in the Netherlands.

Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective Zolt´an Tuba1;2;, Michael C.F. Protor2 & Zsolt Csintalan1 1

Department of Botany and Plant Physiology, Agricultural University of G¨od¨ollo˝, H-2103 G¨od¨ollo˝, Hungary; Department of Biological Sciences, University of Exeter, Hatherly Laboratories, Prince of Wales Road, Exeter, EX4 4PS, UK ( corresponding author) 2

Key words: chlorophyll a+b, CO2 assimilation, desiccation-tolerance mechanism, ecological adaptation, homoiochlorophyllous, poikilochlorophyllous, rehydration, respiration, resynthesis

Abstract There is an apparently stark contrast in ecophysiological adaptation between the poikilochlorophyllous desiccationtolerant (PDT) angiosperm Xerophyta scabrida and homoichlorophyllous desiccation-tolerant (HDT) lichens and bryophytes. We summarise measurements on Xerophyta and on the temperate dry-grassland lichen Cladonia convoluta and the moss Tortula ruralis through a cycle of desiccation and rehydration. Considered in a broad ecological and evolutionary context, desiccation tolerance in general can be seen as evading some of the usual problems of drought stress, and these plants as particular instances drawn from an essentially continuous spectrum of adaptive possibilities – related on the one hand to the physical scale of the plants, and on the other to the time-scale of wetting and drying episodes. Abbreviations: DT = desiccation tolerant; HDT = homoichlorophyllous DT; PDT = poikilochlorophyllous DT Introduction Desiccation tolerance occurs widely in the plant kingdom. It is commonplace among bryophytes and lichens, and is found sporadically among vascular plants of diverse taxonomic affinities. Desiccationtolerant plants can survive the loss of 80-95% of their cell water, so that the plants appear completely dry and no liquid phase remains in their cells; after a shorter or longer period in the desiccated state, they revive and resume normal metabolism when they are remoistened. This is a qualitatively different phenomenon from drought tolerance as ordinarily understood in vascular-plant physiology; indeed desiccation tolerance could be seen as a drought-avoiding mechanism in the sense of Levitt [25]. Desiccation-tolerant (DT) plants may be subdivided into homoiochlorophyllous (HDT) and poikilochlorophyllous (PDT) types. The HDTs (which

are the majority) retain their chlorophyll on desiccation, whereas in PDTs desiccation results in the loss of chlorophyll, which must be re-formed following remoistening [2, 10, 11, 12, 14, 15, 43, 50]. Much has been published on the photosynthetic responses of HDT plants, especially on the cryptogamic plants [2, 20, 21, 22, 28, 33, 34, 41, 44]. A good deal of information is available on the tolerance limits of both HDT and PDT desiccation-tolerant phanerogams [10, 11, 42]. However, until our recent studies [4, 48, 49, 50, 51, 53] little was known about the extent and dynamics of the reconstitution and decomposition of the photosynthetic apparatus and there was an absolute gap in our knowledge of the changes in CO2 assimilation and respiration during the course of revival and drying in PDT plants. As a consequence it was not recognized that the poikilochlorophyllous plants represent another DT strategy which is fundamentally different from the HDT strategy [50]. Even in the relatively well-studied

212 lichens and bryophytes, few comprehensive studies have been made of the overall temporal changes in photosynthesis and respiration during a desiccation – rehydration cycle. HDT and PDT plants represent apparently contrasting strategies to solve the same ecological problem. Our aims in this paper are two. First, we outline essential features of representatives of these two patterns of adaptation, as illustrated by our own ecophysiological work on the tropical African PDT monocot Xerophyta scabrida, and two cryptogamic HDT species of central-European dry grasslands, the lichen Cladonia convoluta and the moss Tortula ruralis. Second, we consider how far PDT and HDT plants do indeed represent contrasting strategies, or whether, in a broad ecological and evolutionary context, they may be seen as parts of a common adaptive pattern.

Xerophyta, Tortula and Cladonia: ecophysiological comparisons and contrasts Xerophyta scabrida (Pax) Th., Dur. et Schinz, is a member of the family Velloziaceae (Velloziales, related to the Bromeliales). It is a C3 PDT tropical pseudoshrub, c. 0.4–0.9 m in height, with perennial leaves. On the top of cliffs it forms a semi desert-like bush vegetation on rocks with a long dry season of 5–6 months [32]. Our measurements were made on air-dried leaves collected at the end of the dry season in the Uluguru Mts., Tanzania: the results therefore relate only to physiological responses of the leaf tissues, and not to the responses of the plant as a whole for which a somewhat longer time-scale might be expected. The green-algal (Trebouxia) lichen Cladonia convoluta (Lam.) P. Cout. Vain. and the acrocarpous moss Tortula ruralis (Hedw.) Gaertn et al. ssp. ruralis [see also 52] commonly grow as low patches in dry open sandy grasslands in central Europe, locally forming a substantial part of the ground cover. Our material was collected near F¨ul¨oph´aza, 70 km SSE of Budapest, Hungary. Laboratory methods, and further details of sites and species, are given by Tuba [47], Tuba et al. [48, 49, 50, 51, 52]. A poikilochlorophyllous angiosperm, Xerophyta scabrida The total absence of chlorophyll, chlorophyll fluorescence signals and CO2 assimilation in the desiccated state and until 10 h after the beginning of rehydration

Figure 1. Change of chlorophyll a + b content (mg g 1 d.w.) in the leaves of PDT X. scabrida, HDT T. ruralis shoots and HDT C. convoluta thalli during desiccation (filled symbols) and rehydration (open symbols).

(Figure 1) indicate that the photosynthetic apparatus in X. scabrida is completely lost during desiccation. This is confirmed by our investigations on chloroplast ultrastructure in X. scabrida [49] and those of Sherwin & Faffant [43] on X. viscosa, and by other ultrastructural studies on PDT plants [13, 16]. Following re-moistening, leaves of X. scabrida regained turgor in 6 h and maximum leaf water content within 12 h. The initial period of increased respiration after remoistening (‘rehydration respiration’) was prolonged (lasted up to 30 h); dark respiration returned to normal levels only after 30 h or more [4, 51]. Resynthesis of chlorophylls and carotenoids started 10–12 h after rehydration and normal levels of photosynthetic pigments were attained within 72 h. Net CO2 assimilation became positive 24 h after rehydration and normal rates were reached after 72 h (Figure 2). By this time, all the photosynthetic parameters investigated (thylakoid actvity, stomatal conductance, intercellular CO2 concentration) showed values consistent with normal functioning, and the chloroplasts showed similar ultrastructure to those of fully developed leaves of normal non-DT C3 plants. Under our laboratory conditions X. scabrida leaves took 16-days to dry out completely – six times longer than reported for other PDT plants desiccating in their natural habitats [10]. But this extremely long time was still not enough length to bring about the complete loss of chlorophyll that occurs in the natural habitat of X. scabrida. This indicates that in natural habitat the desiccation period leading to the complete breakdown

213 piration which occurs through the drying-out period is termed desiccation respiration [51, 53]. Two homoiochlorophyllous plants, Tortula ruralis and Cladonia convoluta

Figure 2. Resumption of CO2 assimilation (solid lines) and respiration (dotted lines) in air-dried, achlorophyllous leaves of PDT X. scabrida (in mol m 2 s 1 ) and air-dried HDT moss T. ruralis and lichen C. convoluta (in mol kg 1 s 1 ) during rehydration.

Figure 3. Changes and loss of CO2 assimilation (solid lines) and respiration (dotted lines) in photosynthetically fully active leaves of PDT X. scabrida (mol m 2 s 1 ) and shoots of HDT T. ruralis and thalli of HDT C. convoluta (mol kg 1 s 1 ) during drying out.

of the chlorophylls is longer than 16 days, a conclusion supported by the field observations of T. P´ocs (pers. comm.). During this long period of drying net CO2 assimilation declined sharply, and ceased altogether after day 3 (Figure 3). The reduction in net CO2 assimilation was associated with breakdown in chlorophyll and carotenoid content, reduction in photochemical activity and stomatal closure. Respiration was much less affected than photosynthesis during the desiccation period and was detectable until drying out was almost complete. This may be seen as enabling X. scabrida to maintain the energy supply needed for controlled breakdown of photosynthetic pigments and change of the chloroplasts into desiccoplasts. This res-

In these species the chlorophyll and carotenoid content remained unchanged through the complete desiccation – rehydration cycle (Figure 1). Chloroplast ultrastructure studies on Tortula ruralis [54 and our own unpublished results] are consistent with the conclusion that the photosynthetic apparatus remains essentially intact throughout, as has been reported for other HDT plants [27, 29]. T. ruralis and C. convoluta regained their normal water content within a few minutes of remoistening. Both species resumed respiration immediately on rehydration and the high intensity rehydration respiration [3, 45] was over within 30 min.; respiration then became substantially steady for the remaining 90 min. of the measurements [26, 52]. CO2 assimilation resumed rapidly after rehydration, reflecting the fact that these species preserve their photosynthetic system essentially intact during desiccation [40, 52]. The CO2 compensation point was reached in both species within 5–10 minutes (Figure 2), and normal rates of CO2 assimilation were reestablished within an hour. The restoration of photosynthetic activity was also indicated by slow chlorophyll-fluorescence parameters which returned within 30 min. to predesiccation levels. Both species attained a positive carbon balance within 20 min of remoistening in spite of high levels of dark respiration. Both T. ruralis and C. convoluta dried rapidly. Drying in natural habitats may take from a few minutes to a few hours depending on environmental conditions. In our experiments, which aimed to provide near-natural conditions, desiccation was complete in 150 min in C. convoluta, and 180 min in T. ruralis. As they dried from an oversaturated state, both species showed an initial increase of net CO2 uptake (due to removal of the high diffusion resistance of the excess water), which then declined as the plants dried out, going briefly negative before desiccation was complete. Chlorophyllfluorescence measurements showed a high level of photochemical activity until the plants were almost dry, underlining again that the thylakoids and pigment system is preserved essentially intact through desiccation [52]. Photochemical activity ceased synchronously with CO2 assimilation. Dark respiration remained unchanged up to the time that net CO2 assimilation

214 began to decline. From that point onwards, there was a progressive decline in dark respiration, roughly parallelling the decline in photosynthesis, but continuing beyond the point at which photosynthesis ceased to be detectable (Figure 3; [52]).

Some thoughts on the distribution and nature of desiccation tolerance The wide occurrence of desiccation tolerance has been remarked upon already. In addition to the plant groups in which we tend to be most aware of it, it is common among microorganisms, in many algae, it occurs in such animal groups as the rotifers, nematodes and tardigrades and in crustacea of seasonal water bodies. And of course it is the norm in angiosperm pollen and seeds. It is thus a widely expressed potentiality of living organisms. Generally, in desiccation tolerant algae (including the photobionts of lichens) and bryophytes, the photosynthetic apparatus remains essentially intact through each drying and re-wetting cycle. In angiosperm seeds, the cotyledons of the young embryo are typically bright green, but lose most or all of their chlorophyll as the seed ripens and dries out, to regain chlorophyll and photosynthetic capacity following rehydration and germination. We take this for granted in seeds, and are only surprised at chlorophyll loss and subsequent regreening when we encounter it in the vegetative tissues of an adult plant. It is easy to see desiccation tolerance as an extreme form of drought tolerance. But this may be quite the wrong way to look at it. Desiccation tolerance posses adaptive problems, but they are not the same as the problems of the vascular plant faced with maintaining turgor and cell function under water stress. Desiccation-tolerant plants are in a real sense evading many of the usual problems of drought stress, at the cost of some physiological ‘trade-offs’ [30]. Bryophytes are C3 plants [1, 35], as is Xerophyta scabrida, with a typical C3  13 C value of –27.3‰; they make few concessions to water-use efficiency, but simply suspend metabolism when water is not freely available.

Considerations of scale The optimal adaptation for an organism depends critically on scale. Raven [37] has emphasised the essential role of supracellular transport systems – xylem and phloem – in the evolution of a land vegetation.

But this is primarily a limitation for the evolution of large land plants, which require highly organised internal conducting systems to maintain the integrated functioning of a bulky plant body in the presence of steep external water-potential gradients. For small plants with a far lower ratio of mass to linear dimension and surface area, a diffuse conducting system (which may be external), may be as good or better and for these small plants, poikilohydry and desiccation tolerance may be an easy adaptive option. For vascular plants, larger physical scale and greater anatomical complexity probably impose limits on the possible time-scale of response to wetting and drying events. It is interesting that some large bryophytes, Polytrichaceae and Dawsoniaceae, have well-developed internal conducting systems approaching the vascularplant pattern, while some small pteridophytes, such as Hymenophyllum, and some small ferns and Selaginella species of intermittently dry habitats [9, 31, 46], appear to rely little on internal conduction and approach the typical bryophyte pattern in their ecological adaptation.

Ecological contexts and adaptive options How do our apparently starkly contrasting pair of examples fit into the larger picture? They have in common desiccation tolerance, and make the general point that this permits colonisation of habitats inaccessible to perennial vascular plants because they are hard and impenetrable roots, or for other reasons cannot provide a year-round supply of water. But they contrast greatly in the time-scale of wetting and drying events to which they are adapted – a time scale measured in weeks or months for Xerophyta, while Tortula and Cladonia can utilise moist periods lasting only an hour or two. This comes near to representing the extremes of a spectrum of possibilities, of which the literature offers examples of many intermediate stages, as in the lichens studied by Ried [38, 39], and the bryophytes studied by Dilks & Proctor [5, 7]. In general, vascular DT plants are adapted to longer drying/wetting cycles than bryophytes or lichens, and when fully hydrated often function as essentially ‘normal’ higher plants. It general too, HDT vascular plants, such as the pteridophytes Selaginella lepidophylla [9] and Ceterach officinarum [31, 42], or angiosperms such as Raymonda mykoni, Craterostigma spp. and Myrothamnus flabellifolia [18, 42, 43] are adapted to more rapid alternations of wet and dry periods than PDT species such as the Xerophyta spp. and

215 Borya nitida. There is variation within each category; thus the herbaceous Craterostigma wilmsii responds more rapidly than the woody Myrothamnus flabellifolia [43]. Of course the categories overlap in their ecological adaptation, and two or more may coexist in one habitat [17]. Both ends of this ecological spectrum have particular points of interest. In Xerophyta (representing the ‘high inertia’ end) the selective advantage of poikilochlorophylly, in minimising photo-oxidative damage [44] and not having to maintain an intact photosynthetic apparatus through long periods of desiccation, presumably outweighs the disadvantage of slow recovery, and still leaves Xerophyta in permanent possession of a habitat, and at an advantage over ephemerals. The majority of HDT plants in the intermediate part of the range are adapted to periods of drying and remoistening ranging in length from hours to weeks. Some can survive long periods of intense desiccation; Racomitrium lanuginosum and Andreaea rothii survived a year’s desiccation at 32% r.h. [5, 6], and Keever [19] reported recovery of Grimmia laevigata from dried herbarium material after 7–10 years. Recovery of full photosynthetic function after normal periods of drying typically takes from a few hours to a day [5, 7]; in many species the morphology of the plant allows for considerable storage of water after rain [8, 36]. The bryophytes and lichens at the ‘low-inertia’ extreme can utilise small amounts of water, during short moist periods, because of their combination of quick recovery and small volume; the cells are typically small, and much of the water associated with the plant is held outside the cells, so a large proportion can be lost before cell function is affected. This pattern of adaptation is seen in the various Negev Desert lichens [23, 24] which can maintain a positive carbon balance during the dry summer season from the short early-morning moist periods provided by dew. Our work (unpublished data) indicates that, although the main periods of growth of Tortula ruralis and Cladonia convoluta in Hungarian dry grasslands are in spring and autumn, they too attain a positive carbon balance from dewfall on clear summer nights.

PHARE/ACCORD (Budapest), Hungarian Scientific Research Foundation (OTKA F-5359, T-017438), British-Hungarian Cooperation in Science and Technology Programme (GB-38/96 Project) and Soros Foundation (Budapest) is gratefully acknowledged.

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