Figure 3. a. Chemical structures of cycad derived specialized
metabolites found in leaves and coralloid roots: (1) BMAA, (2)
Macrozamin and (3) cycacin. (4) hormogonium-inducing factor (HIF)
1-palmitoyl-2-linoleoyl-sn-glycerol produced in precoralloid roots. b.
Chemical structures of microbiota derived metabolites found in coralloid
roots: (5) Caulobacter- produced indigoidine-like metabolite, (6)
cyanobiont produced desmamide A, (7) nostocyclopeptide A1/A3. Note that
BMAA (1) is also produced by cyanobacteria in the coralloid roots. c.
Host genome gene count differences between the coralloid roots (with
Cyanobacteria) vs precoralloid roots (without Cyanobacteria) ofCycas panzhihuaensis. KEGG mapping of enriched genes in coralloid
roots (>10000 counts) correspond to endopeptidase inhibitor
activity (CYCAS_000803, CYCAS_008980, CYCAS_000805), manganese ion
binding and nutrient reservoir activity (CYCAS_020515), response to
stress, stimulus or wounding (CYCAS_000805), and Serine-type
endopeptidase inhibitor activity (CYCAS_000805). Enriched genes in
precoralloid roots (>10000 counts) correspond to
endopeptidases inhibitor activity (CYCAS_018813, CYCAS_001064,
CYCAS_008980). Data from Liu et al . (2022).
Regarding the community ecology of the coralloid, recent studies have
confirmed the existence of multiple microorganisms including fungi and
viruses inside the coralloid root and other nitrogen-fixers such as
Hyphomicrobiales (Rhizobiales) (Bustos-Diaz et al ., in review and
references therein;). While the cyanobiont appears to be the main
nitrogen fixer, the role of the microbial community is not well
characterized, although efforts are underway (Liu et al ., 2023;
Ndlovu et al ., 2023). Along these lines, specialized metabolites
produced under nitrogen starvation by associated bacteria in interaction
with the cyanobiont in Dioon edule have been reported
(Gutiérrez-García et al ., 2019). It has also been suggested that
the community itself might be recruited from the soil as a consortia
because coralloid root microbial composition differs greatly from other
tissues and the surrounding rhizosphere (Suárez-Moo et al ., 2019;
Zheng & Gong, 2019). Investigations into the recruitment of the
community, the possibility of some taxa inherited via the seed, and the
dynamics within coralloid roots are still in their infancy and will
likely produce many important advances in symbiosis ecology and
specialized metabolism in the coming decade.
The long standing hypothesis that coralloid roots are an ancestral
trait, based on the near ubiquity of coralloid roots in all living cycad
species, was recently challenged. In the absence of coralloid root
fossils, a proxy method used to deduce the existence of symbiotic
nitrogen fixation using nitrogen isotopic ratios of fossil cycad leaves
found independent origins of the symbiosis in living Zamiaceae and
Cycadaceae (Kipp et al ., 2024). The authors concluded that a 35
million year old fossil Zamia entered in symbiosis with
nitrogen-fixing bacteria, while inconclusive results were obtained fromBowenia leaf fossils from 50 million years ago. Interestingly,
older fossils from extinct cycad genera showed no signs of being capable
of symbiotic nitrogen fixation. The authors hypothesize that
morphological similarities between coralloid roots from cycads in both
families result from convergent evolution which, if true, would make
cycads a rich system for investigations into plant morphology and
evo-devo. Combined with the ongoing and recent advances in the chemical
ecology and genetics of symbiosis described above, these data provide a
full picture of the ecology, evolution, physiology, genetics, and
development of root symbiosis.
Table 1. Twenty-four conserved cyanobacterial symbiotic associated genes
shared among C. panzhihuaensis , the ferns Azolla
filiculoides and Azolla cf. caroliniana , the liverwortBlasia pusilla and the hornwort Anthoceros punctatus . Gene
sequences can be downloaded from
(https://db.cngb.org/codeplot/datasets/PwRftGHfPs5qG3gE),
data from Liu et al ., (2022).