Vegetative tissues

Desiccation tolerance appears common though not universal in bryophytes (e.g. Richardson, 1981; Proctor, 1990), common in lichens (Kappen and Valladares, 1999), uncommon in pteridophytes and rare in angiosperms (Chapter 7). No gymnosperms are known to tolerate desiccation (Gaff, 1980; Chapter 7), even though gym-nosperms may have desiccation-tolerant seeds or pollen (Chapters 5 and 6). Desiccation tolerance occurs in non-lich-enized fungi, cyanobacteria and algae (Ried, 1960; Mazur, 1968; Bertsch, 1970; Schonbeck and Norton, 1978; Potts, 1994, 1999; Dodds et al., 1995) but little is known about its extent. It must be very common in free-living algae and bacteria that grow on the surface of plants or soil, where they are very probably subject to desiccation.

Different vegetative parts of a plant may have different degrees of tolerance. There seem to be two main patterns. First, in some species only the perennating structures survive desiccation, such as corms in Limosella grandiflora (Gaff and Giess, 1986) or special dry-season organs in the small shrub Satureja gilliesii (Montenegro et al., 1979). As in plants that are desiccation-sensitive but have desiccation-tolerant seeds, tolerance in these species is confined to relatively inactive plant parts. Second, leaves may be more desiccation-tolerant when younger. Younger leaves are more tolerant than older ones in Chamaegigas intre-pidus (Gaff and Giess, 1986) and some species of Borya (Gaff, 1989). In the leaves of some grasses, only the basal meristem-atic zone tolerates drying (Gaff and Sutaryono, 1991). This suggests that some tissues may lose tolerance as they differentiate or age; the processes involved could conceivably parallel those that cause loss of tolerance after germination of seeds. In all these examples of differential tolerance in leaves, there are congeners whose leaves remain tolerant as they mature, offering inviting systems for comparative studies of the ecology and mechanisms of desiccation tolerance.

No one appears to have assessed the relative prevalence of desiccation tolerance in different taxa of bacteria, cyanobacteria, fungi and algae. Acinetobacter radioresis-tans survives 150 days at 31% relative humidity, which helps make it a persistent source of infection in hospitals (Jawad et al., 1998). At least 400 species of algae and cyanobacteria tolerate desiccation (e.g. Davis, 1972; Potts, 1994, 1999; Trainor and Gladych, 1995). Evans (1959) found that many but not all of the freshwater algae in pond mud survived desiccation in the field; at least two species survived 69 days of desiccation in the laboratory without forming resting stages. Two interesting phenomena that have been reported from some green algae but apparently not from other groups are dependence of tolerance on nutrient availability (McLean, 1967, cited in Chandler and Bartels, 1999) and loss of capacity to reproduce after desiccation (Hsu and Hsu, 1998). We know of few reports of desiccation tolerance in non-lichenized fungi (Bisby, 1945; Zimmermann and Butin, 1973), but there is an extensive literature on tolerance in lichens, at least 50 species of which have been shown to tolerate desiccation (Kappen and Valledares, 1999).

Desiccation tolerance is broadly but unevenly distributed among taxa in plants. Most of the 25,000-30,000 species of bryophytes probably tolerate at least brief desiccation of low intensity (Chapter 7); the proportion of desiccation-tolerant species appears to differ between orders of mosses and to be higher in mosses than in liverworts. There are also desiccation-tolerant hornworts (Oliver et al., 2000).

Porembski and Barthlott (2000) estimated that there are 275-325 desiccation-tolerant species of vascular plants. At least nine families of pteridophytes and seven families of angiosperms contain desiccation-tolerant sporophytes (Chapter 7). Some fern gameto-phytes also tolerate desiccation (e.g. Pence, 2000). Groups of ferns and allies that seem to be relatively rich in desiccation-tolerant species include the family Pteridaceae and the genera Cheilanthes and Selaginella (Gaff, 1977; Gaff and Latz, 1978; Kappen and Valladares, 1999; Porembski and Barthlott, 2000). Desiccation-tolerant monocotyledons outnumber tolerant dicotyledons. The monocotyledonous family Velloziaceae may have over 200 tolerant species (Kubitzki, 1998). At least 39 species of Poaceae tolerate desiccation (Gaff, 1997). One very small family of angiosperms, the Myrothamnaceae, is entirely desiccation-tolerant (Porembski and Barthlott, 2000). At the other extreme, some species, such as Borya nitida (Liliaceae), contain both tolerant and sensitive individuals (Gaff, 1981). Phylogenetic analysis suggests that desiccation tolerance in active phases of the life cycle has evolved at least eight separate times in vascular plants (Oliver et al., 2000).

Desiccation-tolerant angiosperms are also widely but unevenly geographically distributed. They occur on all continents except Antarctica, but very few species are known from Europe or North America. The European species are all in two genera from one family (Ramondia and Haberlea in the Gesneriaceae) (Muller et al., 1997; Drazic et al., 1999). The North American species include three grasses (Iturriaga et al., 2000). The greatest concentrations of known desiccation-tolerant angiosperms are in southern Africa, western Australia and eastern South America (Figs 1.1 and 1.2; Gaff, 1977, 1987; Gaff and Latz, 1978; Porembski and Barthlott, 2000). Different taxa predominate in each of these three areas.

Desiccation-tolerant plants have a wide range of morphological and physiological characteristics (Porembski and Barthlott, 2000). There are desiccation-tolerant annuals and perennials, graminoids and forbs, and herbs, shrubs and arborescent rosette plants. Tolerant species may be caespitose, stolonif-erous or rhizomatous. Some species are xero-morphic, such as B. nitida (Gaff and Churchill, 1976); others are not, such as Boea hygroscopica (Gaff, 1981). A few desiccation-tolerant species, like C. intrepidus, have morphological features typical of aquatic plants (Gaff and Giess, 1986), and at least one species is succulent (Barthlott and Porembski, 1996). Desiccation-tolerant angiosperms can have crassulacean acid metabolism (Barthlott and Porembski, 1996;

Fig. 1.1. Southern Africa is a centre of diversity for desiccation-tolerant angiosperms, including (a) Craterostigma wilmsii, (b) Xerophyta viscosa, (c) Xerophyta retinervis, and (d) Myrothamnus flabellifolius. Each is shown in its desiccated (left) and hydrated (right) state. (Photos by J. M. Farrant.)

Fig. 1.1. Southern Africa is a centre of diversity for desiccation-tolerant angiosperms, including (a) Craterostigma wilmsii, (b) Xerophyta viscosa, (c) Xerophyta retinervis, and (d) Myrothamnus flabellifolius. Each is shown in its desiccated (left) and hydrated (right) state. (Photos by J. M. Farrant.)

Fig. 1.2. The large, isolated, granitic or gneissic outcrops known as inselbergs are a major habitat for desiccation-tolerant vascular plants in Australia, Brazil and Africa. (a) An inselberg in the Mata Atlantica of Brazil; (b) a mat of the pteridophyte Selaginella sellowii on a Brazilian inselberg; (c) an arborescent Brazilian monocot (Velloziaceae); (d) a species of Borya (Boryaceae, shown desiccated) in Australia; (e) Afrotrilepispilosa (Cyperaceae, shown desiccated), a dominant, mat-forming species on inselbergs in West Africa. (Photos by S. Porembski.)

Fig. 1.2. The large, isolated, granitic or gneissic outcrops known as inselbergs are a major habitat for desiccation-tolerant vascular plants in Australia, Brazil and Africa. (a) An inselberg in the Mata Atlantica of Brazil; (b) a mat of the pteridophyte Selaginella sellowii on a Brazilian inselberg; (c) an arborescent Brazilian monocot (Velloziaceae); (d) a species of Borya (Boryaceae, shown desiccated) in Australia; (e) Afrotrilepispilosa (Cyperaceae, shown desiccated), a dominant, mat-forming species on inselbergs in West Africa. (Photos by S. Porembski.)

Markovska et al., 1997) and probably C4 photosynthesis (Lazarides, 1992). However, no plants more than 3 m tall and hence no trees are known to tolerate desiccation, possibly because they cannot re-establish upward movement of water once the xylem cavitates during desiccation (e.g. Sherwin et al., 1998).

The wide distribution of desiccation tolerance in plants has suggested to some authors that the basic mechanism of tolerance must be simple (Chandler and Bartels, 1999). According to the 'water replacement hypothesis' of Crowe et al. (1998a), the evolution of desiccation tolerance in all organisms depends on the selection and synthesis of sufficient concentrations of molecular substitutes for water (Clegg, 2001). Under certain circumstances, tre-halose may even induce desiccation tolerance in human cells (Guo et al., 2000). However, tolerance in plants also involves other mechanisms (Section 1.6), and the ecology of desiccation-tolerant plants suggests that the evolution of tolerance in plants is constrained by its consequences for growth and competition.

+1 0

Post a comment