Isoprenoid Emission in Hygrophyte and Xerophyte European Woody Flora: Ecological and Evolutionary Implications
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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2014) 23, 334–345 bs_bs_banner RESEARCH Isoprenoid emission in hygrophyte and PAPER xerophyte European woody flora: ecological and evolutionary implications Francesco Loreto1*, Francesca Bagnoli2, Carlo Calfapietra3,4, Donata Cafasso5, Manuela De Lillis1, Goffredo Filibeck6, Silvia Fineschi2, Gabriele Guidolotti7, Gábor Sramkó8, Jácint Tökölyi9 and Carlo Ricotta10 1Dipartimento di Scienze Bio-Agroalimentari, ABSTRACT Consiglio Nazionale delle Ricerche, Piazzale Aim The relationship between isoprenoid emission and hygrophily was investi- Aldo Moro 7, 00185 Roma, Italy, 2Istituto per la Protezione delle Piante, Consiglio Nazionale gated in woody plants of the Italian flora, which is representative of European delle Ricerche, Via Madonna del Piano 10, diversity. 50019 Sesto Fiorentino (Firenze), Italy, Methods Volatile isoprenoids (isoprene and monoterpenes) were measured, or 3 Istituto di Biologia Agroambientale e data collected from the literature, for 154 species native or endemic to the Medi- Forestale, Consiglio Nazionale delle Ricerche, terranean. The Ellenberg indicator value for moisture (EIVM) was used to describe Via Marconi 3, Porano (Terni), Italy, plant hygrophily. Phylogenetic analysis was carried out at a broader taxonomic scale 4Global Change Research Centre – CzechGlobe, on 128 species, and then refined on strong isoprene emitters (Salix and Populus Belidla 4a, 603 00 Brno, Czech Republic, species) based on isoprene synthase gene sequences (IspS). 5Dipartimento di Biologia, Università degli Studi di Napoli ‘Federico II, Complesso Results Isoprene emitters were significantly more common and isoprene emis- Universitario di Monte S. Angelo, Via Cinthia, sion was higher in hygrophilous EIVM classes, whereas monoterpene emitters were 80126 Napoli, Italy, 6Dipartimento di Scienze more widespread and monoterpene emission was higher in xeric classes. However, e Tecnologie per l’Agricoltura, le Foreste, la when controlling for phylogeny, isoprene emission was not associated with EIVM, Natura e l’Energia, Università degli Studi della possibly due to the large presence of Salicaceae among hygrophilous isoprene Tuscia, Via San Camillo de Lellis, 01100 emitters. Moreover, the distribution of isoprene emitters among EIVM classes was 7 Viterbo, Italy, Dipartimento per l’ not related to IspS-based phylogenesis in Populus and Salix, suggesting that the Innovazione nei Sistemi Biologici, gene has not undergone evolution linked to ecological pressure. In contrast, Agroalimentari e Forestali, Università degli the monoterpene emission pattern is independent of phylogeny, suggesting that the Studi della Tuscia, Via San Camillo de Lellis, evolution of monoterpenes is associated with transitions to more xeric habitats. 01100 Viterbo, Italy, 8Ecology Research Group, MTA-ELTE-MTM, Pázmány Péter Sétány 1/C, Main conclusions Our results reveal an interesting ecological pattern linking H-1117 Budapest, Hungary, 9MTA-DE isoprenoids and water availability. We suggest that isoprene is a trait that: (1) ‘Lendület’ Behavioural Ecology Research evolved in plants adapted to high water availability; (2) is replaced by more effective Group, University of Debrecen, Egyetem tér 1, protection mechanisms, e.g. more stable isoprenoids, in plants adapting to more H-4032 Debrecen, Hungary, 10Dipartimento di xeric environments; and (3) being strongly constrained by phylogeny, persists in Biologia Ambientale, Università degli Studi Salicaceae adapted to more xeric environments. Roma ‘La Sapienza’, Piazzale Aldo Moro 5, 00185 Roma, Italy Keywords Adaptation, chemo-taxonomy, hygrophytes, isoprene, monoterpenes, *Correspondence: Francesco Loreto, CNR phylogenies, salicaceae, xerophytes, water stress. Dipartimento di Scienze Bio-Agroalimentari, Piazzale Aldo Moro 7, 00185 Roma, Italia. E-mail: [email protected] Schnitzler, 2010). Isoprene and monoterpenes are formed INTRODUCTION during photosynthetic metabolism in the chloroplasts The leaves of many woody and perennial plants constitutively (Loreto & Schnitzler, 2010). Generally, either isoprene or emit volatile isoprenoids (isoprene and monoterpenes) to the monoterpenes are emitted but not both (Harrison et al., 2013). atmosphere at rates that often exceed 1–2% of the photosyn- However, some species (e.g. Myrtales) show significant storage thetic carbon fixation, especially in stressed leaves (Loreto & of monoterpenes in specialized structures and these species DOI: 10.1111/geb.12124 334 © 2013 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/geb Isoprenoid emission in hygrophytes and xerophytes can emit both isoprene and monoterpenes (Niinemets et al., The Ellenberg indicator values (EIVs; Ellenberg, 1974; 2004). Ellenberg et al., 1991) characterize the adaptation of a vascular Isoprene is believed to play a protective role against thermal plant species to edaphic and climatic conditions in comparison and oxidative stresses, possibly because of the capacity of this with other species; i.e. each plant species is given values denoting molecule to stabilize thylakoidal membranes (Singsaas et al., the position at which plants reach peak abundance along envi- 1997; Velikova et al., 2011), or to remove reactive oxygen or ronmental gradients (Diekmann, 2003; Godefroid & Dana, nitrogen species within the mesophyll (Loreto & Velikova, 2001; 2007). A 9- or 12-point ordinal scale for each of the following Vickers et al., 2009). Light-dependent monoterpenes may have parameters is used: moisture, soil nitrogen status, soil pH, soil similar roles, but they are also often involved in the communi- chloride concentration, light, temperature and continentality. cation of plants with other organisms, especially in multitrophic Although EIV were originally designed for central Europe and plant defence and pollination (Dicke & Baldwin, 2010). assigned to the central European flora only (Ellenberg, 1974; The emission of isoprene and monoterpenes is widespread Ellenberg et al., 1991), they have been subsequently redefined across plant families (Harley et al., 1999). A recent study has and calculated for other floras, such as those of Britain (Hill indicated a strong phylogeographic signal for monoterpenes; the et al., 1999), southern Greece (Böhling et al., 2002) and Italy emission of monoterpenes is qualitatively different in cork oaks (Pignatti et al., 2005). EIVs have been widely used to interpret across their distribution range in Europe (Loreto et al., 2009). responses to environmental gradients (Diekmann, 2003), and Alien species of Hawaii emit more monoterpenes than native are now also used as an effective tool for applied purposes, such ones, and this has been suggested to be an indication of greater as remotely sensed vegetation monitoring (Schmidtlein, 2005), evolutionary success of alien species since monoterpene emission conservation strategies (Sullivan et al., 2010), ecological resto- is associated with higher stress resistance (Llusiá et al., 2010). ration (Krecek et al., 2010) and prediction of the effects of pol- However, there seems to be no straightforward relationship lution (Jones et al., 2007; Duprè et al., 2010). between isoprene emission and plant taxonomy or phylogeny. Experimental studies found that EIV ranking within a given Isoprene emission is absent in herbaceous, annual vegetation, flora is a highly reliable indicator of adaptation to environmen- whereas it is widespread in trees and perennial plants tal conditions (Schaffers & Sýcora, 2000; Diekmann, 2003; (Kesselmeier & Staudt, 1999). However, this robust trend may Schmidtlein, 2005; Jones et al., 2007; Klaus et al., 2012): in par- not be associated with phylogeny, as isoprene emission is limited ticular, the index for soil moisture (EIVM) was found to to woody life-forms of families that also include herbaceous perform the best (Schaffers & Sýcora, 2000; Fanelli et al., 2007; species (Fineschi et al., 2013). Hanson et al. (1999) reported that Krecek et al., 2010). The EIVM was therefore used here to rank isoprene emission is more widespread in mosses than in all isoprenoid-emitting species of the Italian woody flora according other taxa, and this is so far the only unambiguous phylogenetic to an index of hygrophily. pattern. This finding led to the suggestion that the isoprene Two phylogenetic analyses were carried out on this dataset at emission trait evolved when plants conquered the land and different taxonomic scales. The first analysis was performed at a started coping with more severe thermal extremes than in the broad scale on woody species belonging to 31 different orders water-buffered environment (Hanson et al., 1999). Similarly, representing the main lineages among woody plant species, Vickers et al. (2009) and Fineschi & Loreto (2012) commented to assess whether isoprenoid emissions and EIVM show a that isoprene could have evolved as an initial mechanism to cope phylogenetic signal (i.e. whether phylogenetically related species with more recurrent and stronger oxidative stress in the terres- tend to have more similar EIVM and/or isoprenoid emission trial than in aquatic environments, and was then replaced by values than more distantly related species). The second analysis more effective mechanisms when plants adapted to more xeric was performed on a narrower range of taxa to assess whether conditions. No other adaptive relationships are apparent when changes of the coding sequences for isoprene synthase (IspS), dealing with volatile isoprenoids emitted from plants that