Chemical ecology of symbioses in cycads, an ancient plant lineage

Abstract

Cycads are an ancient lineage of gymnosperms that maintain a plethora of symbiotic associations from across the tree of life. They have myriad morphological, structural, physiological, chemical, and behavioral adaptations that position them as a unique system to study the evolution, ecology, and mechanism of symbiosis. To this end, we have provided an overview of cycad symbiosis biology covering insects, bacteria, and fungi, and discuss the most recent advances in the underlying chemical ecology of these associations.

Keywords: chemical ecology; cyanobacteria; cycads; gymnosperms; microbiome metabolites; plant secondary metabolites; symbiosis; volatile organic compounds.

Fig. 1

Conceptual summary of cycad chemical ecology research presented in this review. Obligate brood‐site pollinators are manipulated by cyclical changes in cone scent chemistry (volatile organic compound (VOC)) that drive a push‐pull pollination mechanism that has existed since at least the mid‐Jurassic. Cycads have highly specialized herbivores, mostly butterfly caterpillars that display aposematic coloring and have, in some cases, been shown to sequester plant secondary metabolites such as methylazoxymethanol glycosides or β‐methylamino‐l‐alanine. Morphologically distinct secondary roots harbor a cyanobacterial‐driven consortium that provides nitrogen (ammonia) to the plant and produces a host of chemical compounds. Most recent research has provided a novel insight on the interaction between the leaf microbiota (fungi and bacteria) and the metabolites produced by the plant and as a product of the interaction. Figure created with Biorender.com (https://BioRender.com/n44v963).

Fig. 2

Examples of cycad mutualistic interactions mediated by chemistry. (a). Zamia furfuracea pollen cone with Rhopalotria furfuracea weevil pollinators. (b). Tranes lyterioides weevil pollinators of Lepidozamia peroffskyana. (c). Gregarious obligate cycad‐feeding Eumaeus atala butterfly larvae show bright red aposematic coloring. (d). Zerenopsis lepida moth larvae are obligate cycad feeders in their first instar and may subsequently shift hosts, yet are also aposematically colored. (e). Young pre‐coralloid roots (prec) in Zamia nana. (f). Fluorescence microscopy of a coralloid root showing the cyanobacterial zone (cyano in red) between the inner and outer cortex. Photo credits: Michael Calonje, Nicholas Fisher, Rolf Oberprieler, Shayla Salzman, Janse van Rensburg et al., , M. Madrid, and J. Ceballos.

Fig. 3

Known and predicted metabolites mediating cycad's symbioses. (a) Chemical structures of experimentally determined cycad‐derived specialized metabolites found in cycads and associated bacteria. Plant metabolites include the toxins macrozamin, cycasin (leaf and roots) and the hormogonium‐inducing factor (HIF) 1‐palmitoyl‐2‐linoleoyl‐sn‐glycerol produced in precoralloid roots to attract cyanobacteria. Symbiotic cyanobacteria produce β‐methylamino‐l‐alanine (BMAA), desmamide A, and nostocyclopeptide A1/A3, and associated Caulobacter produce indigoidine‐like metabolites, all within the coralloid roots. (b) Nostoc phylogeny of cycad cyanobionts with some of the biosynthetic gene clusters (BGCs) that they contain. The uneven distribution suggests that there may not be a universal metabolite associated with symbiosis. The phylogenetic distribution of BGCs is represented on the bacterial phylogeny by the matching color surrounding the chemical products of identified BGCs. (a) was created with Biorender.com (https://BioRender.com/c59s359). (b) was created using data from Bustos‐Diaz et al. (2024).

Fig. 4

Leaf foliar metabolites differ between two ecologically isolated Zamia species. (a). A dendrogram using structural relatedness of foliar metabolites and the relative abundances of each leaf metabolite for the species Zamia nana (terrestrial) and Zamia pseudoparasitica (epiphytic). Zamia foliar metabolites are classified by their biosynthetic pathway as indicated by branch color (natural product classification). The chemical structure of five upregulated metabolites observed for Z. pseudoparasitica is presented. ClassyFire‐specific classification corresponds to N‐acyl‐alpha amino acids, glutamic acid (amino acid) and derivatives, benzodioxoles (shikimate), 1,2‐diacylglycerols (fatty acid), and biflavonoids and polyflavonoids (shikimate) (clockwise). (b). Foliar metabolome composition of Z. nana and Z. pseudoparasitica summarized into two dimensions with nonmetric multidimensional scaling (NMDS) based on pairwise chemical structural‐compositional similarity index, with arrows indicating the correlation (P = < 0.05) between the metabolome and the microbiome. Both figures modified from Sierra et al. (2024) with permission of Springer (License 5985531162609).