Proceedings of the Third International Conference on Invasive ...

Chapter 1: Spartina Biology<strong>Proceedings</strong> <strong>of</strong> <strong>the</strong> <strong>Third</strong> <strong>International</strong> <strong>Conference</strong> on Invasive SpartinaTable 1. Fitness impacts <strong>of</strong> Symbiotic LifestylesLifestyleFitness ImpactHost SymbiontParasitism - +Commensalism 0 +Mutualism + +- = fitness decreased, + = fitness increased,0 = fitness not affectedingress. It appears that when Colletotrichum species areexpressing non-pathogenic lifestyles <strong>the</strong>y are acting asbiological triggers allowing plants to recognize virulentpathogens more quickly (Rodriguez et al. 2004). Theeffectiveness <strong>of</strong> an endophyte as a biological trigger appearsto be a function <strong>of</strong> currently undefined genetic compatibilitywith <strong>the</strong> host.ADAPTIVE SYMBIOSISMutualistic fungi are known to confer a variety <strong>of</strong>fitness benefits. However, it is not known if symbioticallyconferred stress tolerance reflects an adaptive response by<strong>the</strong> host and/or symbiont. We have studied <strong>the</strong> ecologicalsignificance <strong>of</strong> endophytic fungi in plants thriving ingeo<strong>the</strong>rmal soils and found that <strong>the</strong> symbiosis is responsiblefor <strong>the</strong> ability <strong>of</strong> both host and symbiont to survive <strong>the</strong>rmalstress (Redman et al. 2002b; Marquez et al. 2007). In over200 individuals analyzed, <strong>the</strong> plant Dichan<strong>the</strong>liumlanuginosum is colonized by one fungal species (Curvulariaprotuberata) that is known to be a pathogen in o<strong>the</strong>r plantspecies (Farr et al. 1989). The fungal endophyte colonizesroots, crowns, stems, leaves and seed coats but not seeds.When seed coats are removed and seeds’ surfaces aresterilized it is possible to propagate plants devoid <strong>of</strong> <strong>the</strong>fungus. This approach allowed us to compare <strong>the</strong> ability <strong>of</strong>symbiotic and non-symbiotic plants to mitigate <strong>the</strong> impacts<strong>of</strong> <strong>the</strong>rmal stress. Nei<strong>the</strong>r <strong>of</strong> <strong>the</strong> symbiotic partners toleratedtemperatures above 40°C, however, <strong>the</strong> symbiosis allowedboth to survive root temperatures up to 70°C. Recently wehave observed that isolates <strong>of</strong> C. protuberata from nongeo<strong>the</strong>rmalplants do not confer temperature tolerancesuggesting that this is an adaptive response by fungi in <strong>the</strong>geo<strong>the</strong>rmal habitat (Rodriguez et al. 2008).Comparative studies with Colletotrichum andCurvularia species support <strong>the</strong> hypo<strong>the</strong>sis that symbiosesadapt to habitat stresses (Rodriguez et al. 2008). These fungiwere assessed for <strong>the</strong> ability to confer heat tolerance (anabiotic stress in geo<strong>the</strong>rmal habitats) and disease resistance(a biotic stress in agricultural habitats) to host plants.Colletotrichum isolates expressing non-pathogenic lifestylesconferred disease resistance but not heat tolerance.Conversely, Curvularia isolates conferred heat tolerance butnot disease resistance. This observation suggests that at leastsome <strong>of</strong> <strong>the</strong> benefits conferred by mutualistic endophytesappear to reflect habitat-specific adaptation.Colletotrichum species that express a mutualisticlifestyle typically are able to asymptomatically colonizegenetically divergent plant species (Redman et al. 2001). Forexample, C. magna is a virulent pathogen on cucurbits but isa disease protecting mutualist on tomato (Lycopersiconesculentum), beans (Phaseolus vulgaris) and strawberry(Fragaria ananassa), three genetically divergent species.Therefore, it appears that genetically distant plant speciescan gain novel biological function simply by formingsymbioses with different fungi. This could allow individualplant species to make quantum evolutionary leaps andexpand into new habitats or become dominant members <strong>of</strong>existing communities.SYMBIOSIS AS A POTENTIAL MECHANISM OFINVASIVENESSBased on <strong>the</strong> broad host range <strong>of</strong> class 2 fungalendophytes, <strong>the</strong>ir ability to confer abiotic and biotic stresstolerance, and <strong>the</strong> apparent adaptive nature <strong>of</strong> symbioses, wepropose <strong>the</strong> following hypo<strong>the</strong>sis: The conversion <strong>of</strong> at leastsome non-native plants into invasive species requires <strong>the</strong>establishment <strong>of</strong> symbioses with endophytic fungi thatconfer tolerance to abiotic and biotic stresses. Thesesymbioses allow invasive species to circumvent <strong>the</strong>ecological factors that keep native species under control andplant communities balanced. In order to properly challengethis hypo<strong>the</strong>sis (designated <strong>the</strong> “symbiotic communicationhypo<strong>the</strong>sis”) several questions must be addressed such as:Do non-native species carry non-native endophytes whentransported? Are <strong>the</strong> non-native endophytes capable <strong>of</strong>releasing non-native plants from ecological controls? If <strong>the</strong>non-native plants are devoid <strong>of</strong> endophytes what are <strong>the</strong>dynamics <strong>of</strong> colonization by native fungi? If an adaptiveresponse is required before non-native plants becomeinvasive, what are <strong>the</strong> temporal dynamics <strong>of</strong> adaptation?Ano<strong>the</strong>r mystery <strong>of</strong> plant invasions is that <strong>the</strong>re is a timelag time between introduction and spread which may bemore than 100 years (Binggeli 2000). Several hypo<strong>the</strong>seshave been proposed to explain invasive lag time but nonehave adequately addressed this phenomenon. We havedemonstrated that subtle differences in host genotypes aresufficient to eliminate symbiotically conferred stresstolerance and may result in <strong>the</strong> expression <strong>of</strong> pathogenicra<strong>the</strong>r than mutualistic lifestyles by endophytic fungi(Redman et al. 2001). Therefore, we propose that <strong>the</strong> lagphase commonly observed between introduction andinvasion may reflect one or more <strong>of</strong> <strong>the</strong> following:1) Endophytes carried with non-native plants adapt tonew habitat stresses and confer stress tolerance allowingnon-native plants to outcompete native plants;-40-