Cycad phyllosphere microbiota and interaction with the plant
metabolome
Above-ground plant tissues (i.e., the phyllosphere) microbiota may also
play a role in plant ecology and fitness. Phyllosphere bacteria of
cycads has only been published in Cycas panzhihuaensis(Zheng & Gong, 2019), but did not include leaves, the most prominent
cycad organ. The authors found that reproductive structures (ovules,
unfertilized and viable seeds) contain less bacterial diversity in
comparison with roots (which are enriched in cyanobacteria). Bacterial
communities among reproductive organs were highly similar and dominated
by the family Enterobacteriaceae. Cycad pollen, however, was
significantly enriched with Comamonadaceae, when compared to the other
plant organs (Zheng & Gong, 2019). Here we present the first cycad leaf
bacteriome and mycobiome (Fig. 4a, b). We find that Enterobacteriaceae
are rarely represented in the phyllosphere community of six Zamiaspecies, while Nostocaceae, Beijerinckiaceae and Acetobacteraceae are
abundant. The rather surprising abundance of the nitrogen fixing
bacteria Desmonostoc suggests functional redundancy with
coralloid roots, possibly as a failsafe to ensure the plant acquires
sufficient fixed nitrogen (Moyes et al ., 2016) and represents the
first evidence of potential additional symbionts in these long-lived
plants. Research on leaf fungal endophytes is limited to a few studies,
i.e., Encephalartos (Nesamari et al ., 2017) and twoZamia species (Sierra et al ., in review). The endophytic
leaf fungi form a polyphyletic assemblage of mostly Ascomycota (Fig.
5b). These initial diversity studies of leaf endo- and epiphytic
microbes provide a veritable mine of data for further investigations
into the ecological and evolutionary significance of the phyllosphere.
Cycads are known for harboring a number of anti-herbivore and toxic
compounds (see Sect. V), whose origin and impact across trophic levels
has been a source of great debate (Marler, Snyder & Shaw, 2010 and
reference therein). Sierra et al . (in review) recently addressed
the association of plant-microbiota (bacteria and fungi) on the
intraspecific leaf metabolome composition of two species (Zamia
nana and Z. pseudoparasitica ). Among the 49 abundant
metabolites, five compounds (Benzodioxoles, Biflavonoids and
polyflavonoids, 1,2-diacylglycerols, N-acyl-alpha amino acids and
glutamic acid and derivatives), were more expressed in Z.
pseudoparasitica compared to Z. nana (Sierra et al . , in
review). The metabolite variation was correlated to bacterial and fungal
leaf endophyte community composition (Fig. 4c), and significantly
associated with the abundance of one bacterial order (Frankiales) and
three fungal orders (Hypocreales, Sordariales and Chaetothyriales). We
are just beginning to unravel the association of cycad metabolites with
phyllosphere microbiota and the ecological consequences for associated
insects. Defensive secondary metabolites in cycads seem to be induced by
complex plant-microbe reciprocal interactions, which calls for
experimental research to uncover the genomic and biochemical
underpinnings derived by the host and endophytic microbes, or both.