Co‐evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal

Abstract

Symbioses between the root nodule-forming, nitrogen-fixing actinomycete Frankia and its angiospermous host plants are important in the nitrogen economies of numerous terrestrial ecosystems. Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) analyses of the 16S rRNA-ITS gene and of the nifD-nifK spacer was conducted directly on root nodules collected worldwide from Casuarina and Allocasuarina trees. In their native habitats in Australia, host species contained seven distinctive sets of Frankia in seven different molecular phylogenetic groups. Where Casuarina and Allocasuarina trees are newly planted outside Australia, they do not normally nodulate unless Frankia is introduced with the host seedling. Nodules from Casuarina trees introduced outside Australia over the last two centuries were found to contain Frankia from only one of the seven phylogenetic groups associated with the host genus Casuarina in Australia. The phylogenetic group of Frankia found in Casuarina and Allocasuarina trees introduced outside Australia is the only group that has yielded isolates in pure culture, suggesting a greater ability to survive independently of a host. Furthermore, the Frankia species in this group are able to nodulate a wider range of host species than those in the other six groups. In baiting studies, Casuarina spp. are compatible with more Frankia microsymbiont groups than Allocasuarina host spp. adapted to drier soil conditions, and C. equisetifolia has broader microsymbiont compatibility than other Casuarina spp. Some Frankia associated with the nodular rhizosphere and rhizoplan, but not with the nodular tissue, of Australian hosts were able to nodulate cosmopolitan Myrica plants that have broad microsymbiont compatibility and, hence, are a potential host of Casuarinaceae-infective Frankia outside the hosts' native range. The results are consistent with the idea that Frankia symbiotic promiscuity and ease of isolation on organic substrates, suggesting saprophytic potential, are associated with increased microsymbiont ability to disperse and adapt to diverse new environments, and that both genetics and environment determine a host's nodular microsymbiont.

Diversity of Frankia in root nodules of six Morella sp. from the Cape flora of South Africa

“…Morella is the only extant actinorhizal genus native to southern Africa, as endemic Casuarina became extinct in the middle Miocene (Coetzee and Praglowski 1984;Linder 2003). This study thus provides additional support for the claim that Morella do not serve as a reservoir for typical Casuarina strains in the absence of their normal hosts (Simonet et al 1999). …”

Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography

“…strain HFPCcI3 (CcI3) represents narrow host range Casuarina strains commonly detected in nodules collected from casuarinas in their native Australia ( Fig. 2A) and in areas of the world where casuarina trees have been planted as windbreaks or for erosion control (Simonet et al 1999). Similar strains have not been found in soils in the absence of a suitable host, indicating that the bacteria depend on the plant for their soil propagation (Simonet et al 1999).…”

“…The results of these broad comparisons lead us to propose a link between the biogeographic history of the actinorhizal plants and the genome evolution of the bacterial symbionts. Evidence from ecological (Zimpfer et al 1997), molecular ecological (Simonet et al 1999), physiological (Sellstedt 1995), and now genomic studies indicates that Casuarina strains represented by CcI3 have evolved to become specialists with reduced genomes. Unlike Alnus and Elaeagnus strains, they have not been detected by trapping experiments in soils outside the native ranges of their host plants (Zimpfer et al 1997;Simonet et al 1999), and they infect a narrow spectrum of hosts ( Fig.…”

Diversity of Frankia Populations in Root Nodules of Geographically Isolated Arizona Alder Trees in Central Arizona (United States)

“…Frankia strains infecting Casuarina plants have been shown to have coevolved with their host plant, illustrating the importance of the host plant in shaping the diversity and evolution of these strains (44). However, for most Frankia strains, no simple pattern of coevolution is present (3).…”