Inaugural Sprent Review: Explaining the evolutionary and biogeographical success of nodulated legumes compared with actinorhizal plants

Today our inaugural Sprent Review was published in the March issue of Journal of Ecology. The first Sprent Review is “Evolution and biogeography of actinorhizal plants and legumes: A comparison” by Julie Ardley and Janet Sprent. Here Julie and Janet discuss Janet’s illustrious career in ecology and provide details about their new review paper.

You can find out more about the journal’s new Sprent Review series in this recent post by Senior Editors, Richard Bardgett and David Gibson.

Emeritus Professor Janet Sprent, FRSE, OBE, has made an enormous contribution to the field of symbiotic nitrogen fixation during a long and distinguished scientific career. After receiving a BSc, Associateship of the Royal College of Science (ARCS) from Imperial College London in 1954, Janet worked at Rothamsted Experimental Station, where she met her future husband Peter, an Australian statistician on sabbatical from the University of Tasmania. Following their marriage, Janet returned with Peter to the University of Tasmania, where she began her doctoral studies on the effects of gibberellic acid on tall and dwarf pea genotypes, receiving her PhD in 1960. Peter and Janet accepted positions at the University of Dundee in 1967, where Janet has since performed the bulk of her research and where she was awarded a Personal Chair. In pursuit of her research, Janet has travelled to every continent on the globe and maintains active collaborations with researchers in Australia, Brazil, India, Kenya, Mexico, South Africa and the United States. She has been awarded Honorary Membership of the British Ecological Society, a DSc from London University in 1988 and an honorary Doctorate in Agriculture from the University of Uppsala in 2006. Janet’s first paper was published in Nature in 1957. More than 200 research articles later she continues to publish, mainly focusing on the legume-rhizobia symbiosis and the ecology, biogeography and phylogeny of both the plant hosts and their microsymbiont partners.

Janet Sprent, Dove Lake, Tasmania, 2018. Photo: Julie Ardley

In honour of Janet’s achievements, Journal of Ecology has initiated the Sprent Review series. In this inaugural paper we compare the nitrogen-fixing symbioses of actinorhizal plants and legumes and suggest that characteristic features of the legume-rhizobia symbiosis have contributed to legumes’ evolutionary and biogeographical success.

Nitrogen (N), a critical element required for plant growth, is usually the most limiting nutrient in terrestrial ecosystems. Within the Rosid I clade of angiosperms, some members of the Fagales, Cucurbitales, Rosales and Fabales form specialised organs known as nodules on their roots (or occasionally stems), within which they house diazotrophic bacteria that supply reduced N in the form of ammonia to the plant host in exchange for photosynthetically derived carbon. However, nitrogen fixation has a high energy cost and a recent paper has suggested that a single gain of nodulation was followed by massive parallel losses in diverse lineages within the nitrogen-fixing root nodule (NFN) clade, driven by selection pressure against the energetically expensive process of nitrogen fixation. The loss of the nitrogen fixation trait has not been uniform across the NFN clade though: within the three orders (Cucurbitales, Fagales and Rosales) that contain actinorhizal plant-Frankia symbioses, only some 230 species are nodulators. This contrasts with the Leguminosae-rhizobia symbioses within the Fabales, where only 2,000 or so of the ~19,300 species are confirmed as non-nodulating.

(L) Dipogon lignosus. (R) Mimosa pudica. Photos: Julie Ardley.

We therefore asked the question: in evolutionary terms, why has symbiotic nitrogen fixation, as a trait, been so successful in nodulated legumes compared with actinorhizal lineages? To answer, we first present an overview of the evolution and biogeography of legume and actinorhizal symbioses and then compare the specific features of actinorhizal and legume symbioses. Firstly, there are differences in the microsymbionts. Frankia spp. are free-living diazotrophs, whereas most of the phylogenetically diverse species of rhizobia are unable to fix N2 ex planta. Rhizobial symbiotic genes are contained within mobile genetic elements, allowing diverse bacteria to acquire sym genes via horizontal gene transfer and thereby gain the ability to nodulate a legume host. Legume hosts have also evolved characteristic features that increase their control of the microsymbiont and enhance the efficiency of N2 fixation. Legume nodules are stem-like organs with peripheral vascular systems, whereas actinorhizal nodules are modified lateral roots with a central vascular system. Most legumes contain their microsymbionts within symbiosomes, rather than the infection threads found in actinorhizal nodule cells. Legume hosts within the Inverted Repeat Lacking Clade impose terminal differentiation on their bacteroids. Legumes also have effective processes for autoregulation of nodulation and downregulation of N2 fixation in response to high levels of soil N.

(L) Gompholobium tomentosum. (R) Trifolium purpureum. Photos: Julie Ardley.

We suggest that these characteristic features of the legume-rhizobia symbiosis, specifically legumes’ greater flexibility in the choice of microsymbiont partner and the evolution of features that increase the efficiency of N2 fixation, are factors that can explain why the majority of species within the Leguminosae have retained the ability to nodulate and how this has contributed to their evolutionary success.

Julie Ardley Murdoch University, Australia
Janet Sprent University of Dundee, UK

You can read the first Sprent Review here: Evolution and biogeography of actinorhizal plants and legumes: A comparison

One thought on “Inaugural Sprent Review: Explaining the evolutionary and biogeographical success of nodulated legumes compared with actinorhizal plants

  1. Pingback: Volume 109 Issue 3 | Journal of Ecology Blog

Leave a Reply

Fill in your details below or click an icon to log in: Logo

You are commenting using your account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s