Vol.:(0123456789) 1 3 Acta Physiologiae Plantarum (2022) 44:123 https://doi.org/10.1007/s11738-022-03455-x ORIGINAL ARTICLE Unpigmented lichen substances protect lichens against photoinhibition of photosystem II in both the hydrated and desiccated states Nqobile Truelove Ndhlovu 1  · Farida Minibayeva 2  · Richard Peter Beckett 1,3 Received: 20 November 2021 / Revised: 22 July 2022 / Accepted: 3 September 2022 © The Author(s) under exclusive licence to Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2022 Abstract Lichen secondary metabolites have been suggested to play a great diversity of roles in lichen biology by acting as UV screens, antimicrobials, herbivore deterrents or allelopathic compounds. However, evidence is also beginning to accumulate that in addition to these roles, even faintly pigmented or unpigmented lichen substances can reduce photoinhibition caused by high levels of photosynthetically active radiation (PAR). Here we used an acetone rinsing technique to remove lichen substances from four common epiphytic Afromontane macro lichens, Parmelia perlata, Ramalina celastri, Usnea dasaea, and Het- erodermia leucomela. Results showed that lichen substances can increase the tolerance of lichens to the photoinhibition of PSII of their photobionts when hydrated, apparently by increasing refectance. However, in the feld, lichens may sufer more photoinhibition when fully or partially desiccated. Here we show for the frst time that, except for the atranorin-containing Heterodermia, lichen substances can also protect desiccated lichens. Interestingly, removal of substances has no efect on refectance when lichens are dry, suggesting that lichen substances protect photobionts in other ways. Keywords Secondary metabolites · Light stress · Desiccation · Photoinhibition · Chlorophyll fuorescence Introduction Lichenization involved the development of thalli that nei- ther symbiont could form on their own, enabling lichens to grow in habitats that were previously unavailable to their free-living symbionts. However, in sunny or well-lit areas the photobionts need to tolerate high light intensities, which can cause a temporary or longer-lasting reduction of pho- tosynthesis called photoinhibition (Beckett et al. 2021). It has been well established that in feld situations photoin- hibition is a regular occurrence. For example, Gauslaa and Solhaug (2000) and Jairus et al. (2009) demonstrated that sustained reductions in photosynthesis can occur in tree- inhabiting lichens suddenly exposed to high light e.g., as a result of the felling of surrounding trees. There is a lack of consensus as to the precise mechanism of photoinhibi- tion. However, the majority of workers consider that when photosynthetic organisms absorb more light energy than they can use in photosynthesis, the excess energy activates oxygen producing reactive oxygen species (ROS) (Guru- rani et al. 2015; Pospíšil 2016; Roach and Krieger-Liszkay 2019; Zavafer and Mancilla 2021). In general, poikilohydric organisms are likely to be particularly sensitive to high light stress. Although not specifcally tested for lichens, in drying poikilohydric higher plants phosphorylation can continue after carbon fxation has stopped, and the energy absorbed will increase ROS production (e.g. Georgieva et al. 2007; for review see Challabathula et al. 2018). Furthermore, even though lichens may rapidly dry out when exposed to high light, they can nevertheless be photo-inhibited even when Communicated by K. Jan Strzałka. * Richard Peter Beckett rpbeckett@gmail.com Nqobile Truelove Ndhlovu nqoohndhlovu@gmail.com Farida Minibayeva minibayeva@kibb.knc.ru 1 School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa 2 Kazan Institute of Biochemistry and Biophysics, Federal Research Center, Kazan Scientifc Center of RAS”, PO Box 30, Kazan 420111, Russia 3 Open Lab ‘Biomarker’, Kazan (Volga Region) Federal University, Kremlevskaya str. 18, 420008 Kazan, Russia