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Nitrogen isotopes reveal independent origins of N 2 -fixing symbiosis in extant cycad lineages.

Michael A KippEva E StüekenCaroline A E StrömbergWilliam H BrightlyVictoria M ArbourBoglárka ErdeiRobert S HillKirk R JohnsonJiří KvačekJennifer C McElwainIan M MillerMiriam A SlodownikVivi VajdaRoger Buick
Published in: Nature ecology & evolution (2023)
Cycads are ancient seed plants (gymnosperms) that emerged by the early Permian. Although they were common understory flora and food for dinosaurs in the Mesozoic, their abundance declined markedly in the Cenozoic. Extant cycads persist in restricted populations in tropical and subtropical habitats and, with their conserved morphology, are often called 'living fossils.' All surviving taxa receive nitrogen from symbiotic N 2 -fixing cyanobacteria living in modified roots, suggesting an ancestral origin of this symbiosis. However, such an ancient acquisition is discordant with the abundance of cycads in Mesozoic fossil assemblages, as modern N 2 -fixing symbioses typically occur only in nutrient-poor habitats where advantageous for survival. Here, we use foliar nitrogen isotope ratios-a proxy for N 2 fixation in modern plants-to probe the antiquity of the cycad-cyanobacterial symbiosis. We find that fossilized cycad leaves from two Cenozoic representatives of extant genera have nitrogen isotopic compositions consistent with microbial N 2 fixation. In contrast, all extinct cycad genera have nitrogen isotope ratios that are indistinguishable from co-existing non-cycad plants and generally inconsistent with microbial N 2 fixation, pointing to nitrogen assimilation from soils and not through symbiosis. This pattern indicates that, rather than being ancestral within cycads, N 2 -fixing symbiosis arose independently in the lineages leading to living cycads during or after the Jurassic. The preferential survival of these lineages may therefore reflect the effects of competition with angiosperms and Cenozoic climatic change.
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