Joint dispersal does not imply maintenance of partnerships in lichen symbioses.

Dispersal of symbiotic partners by joint propagules is considered as an efficient strategy to maintain successful associations and to circumvent low symbiont availability. Joint dispersal is widespread in diverse symbioses and a particularly common reproductive mode in lichens. We were interested in the implications of joint symbiont dispersal on population genetic structure and investigated patterns of symbiont association in populations of two closely related lichen species in the genus Physconia, with similar range of compatible algal partners. One of the lichen species is characterized by joint dispersal of both symbionts, whereas the other species propagates by meiotic fungal spores alone. The latter species must reestablish the symbiotic stage with appropriate algae sampled from the environment. Both fungal species have specialized on photobionts representing a monophyletic lineage of the algal genus Trebouxia. The results indicate no correlated association of symbiont genotypes in the species with joint symbiont dispersal. We rather show that algal gene diversity in populations of lichenized fungi with different propagation strategies is not necessarily different. The association with algae that differ from the co-dispersed genotypes during the vegetative development of the thalli is the most likely explanation for the observed pattern. Maintenance of symbiotic associations is an option but not a strict consequence of joint symbiont dispersal in lichens.

Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners.

Extreme desiccation and irradiation increase the formation of reactive oxygen species in organisms. Lichens are highly resistant to potential damage, but it is not known whether biochemical interaction between their fungal and algal partners is involved in conferring stress tolerance. Here, we show that antioxidant and photoprotective mechanisms in the lichen Cladonia vulcani are more effective by orders of magnitude than those of its isolated partners. When alone, both alga and fungus suffer oxidative damage during desiccation, but in the lichen, each appears to induce up-regulation of protective systems in the other. Without the fungal contact, the alga tolerates only very dim light and its photoprotective system is only partially effective; without the alga, the glutathione-based antioxidant system of the fungus is slow and ineffective. In the lichen, this mutually enhanced resistance to oxidative stress and, in particular, its desiccation tolerance are essential for life above ground. This lifestyle, in turn, increases the chance of dispersal of reproductive propagules and ensures their joint evolutionary success.

Biochemical traits of lichens differing in relative desiccation tolerance.

• Oxidative stress arises when desiccation restricts photosynthesis and light energy is transferred from photo-excited pigments onto ground state oxygen. We tested whether a highly desiccation tolerant lichen, Pseudevernia furfuracea, displays better protection against oxidative stress than more sensitive species, Lobaria pulmonaria and Peltigera polydactyla. • We rehydrated lichens after desiccation periods of 2, 7 and 9 weeks and assessed their viability by measuring CO2 exchange using IRGA. During desiccation and rehydration, photosynthetic pigments and the antioxidant α-tocopherol were analysed by HPLC, and peroxidases by spectrophotometry. • Pseudevernia furfuracea contained considerably lower chlorophyll, α-tocopherol and ß-carotene concentrations and peroxidase activity than the two other lichens. However, it recovered photosynthesis rapidly, even after remaining in the desiccated state for 2 months while there was a significant delay in the onset of photosynthesis in L. pulmonaria and P. polydactyla. • We conclude that high antioxidant concentrations do not necessarily indicate better adaptation to desiccation. Rather, the ability to rapidly re-establish the species-specific normal antioxidant concentrations during rehydration, even after longer desiccation times, is a characteristic of well-adapted species.

Revival of a resurrection plant correlates with its antioxidant status.

Myrothamnus flabellifolia, a short woody shrub from southern Africa, can survive severe desiccation of its vegetative organs. We studied mechanisms protecting this plant from oxidative damage during desiccation for 2 weeks, 4 and 8 months, and also during subsequent rehydration. This plant retains high concentrations of chlorophyll during desiccation, and these chlorophyll molecules are probably a source for potentially harmful singlet oxygen production. Desiccation triggered substantial increases in zeaxanthin and redox shifts of the antioxidants glutathione and ascorbate towards their oxidised forms. Simultaneously, the concentrations of violaxanthin, beta-carotene, ascorbate, alpha-tocopherol, and glutathione reductase activity progressively decreased. Antheraxanthin, gamma-tocopherol, lutein, neoxanthin and glucose-6-phosphate dehydrogenase displayed less pronounced changes in response to desiccation. Even after 4 months of desiccation, Myrothamnus flabellifolia recovered rapidly upon rehydration. Re-watering induced formation of ascorbate and glutathione, simultaneous reduction of their oxidised forms, and rapid production of alpha-tocopherol and of various carotenoids. Only after 8 months of desiccation did the antioxidant system of M. flabellifolia break down; 3 weeks after the onset of rehydration, these plants abscised their leaves, but even then they were still able to recover and develop new ones. Ascorbate, beta-carotene and alpha-tocopherol were totally depleted after 8 months of desiccation and did not recover upon rehydration; glutathione was partly maintained, but only in the oxidised form. We present a model demonstrating which parts of antioxidant pathways break down as oxidative stress becomes detrimental and we discuss some potential implications of our results for the genetic modification of crop plants to improve their drought tolerance.